Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots

Khan, Mather A.; Castro‐Guerrero, Norma A.; McInturf, Samuel A.; Nguyen, Nga T.; Dame, Ashley N.; Wang, Jiaojiao; Bindbeutel, Rebecca K.; Joshi, Trupti; Jurisson, Silvia S.; Nusinow, Dmitri A.; Mendoza‐Cozatl, David G.

doi:10.1111/pce.13192

Title: Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots

Journal Article · Thu Mar 08 00:00:00 EST 2018 · Plant, Cell and Environment

DOI:https://doi.org/10.1111/pce.13192· OSTI ID:1610619

Khan, Mather A. ^[1]; Castro‐Guerrero, Norma A. ^[1]; McInturf, Samuel A. ^[1]; Nguyen, Nga T. ^[1]; Dame, Ashley N. ^[1]; Wang, Jiaojiao ^[1];

^[2]; Joshi, Trupti ^[1]; Jurisson, Silvia S. ^[1];

^[2];

^[1]

Univ. of Missouri, Columbia, MO (United States)
Donald Danforth Plant Science Center, St. Louis, MO (United States)

Abstract The OLIGOPEPTIDE TRANSPORTER 3 (OPT3) has recently been identified as a component of the systemic network mediating iron (Fe) deficiency responses in Arabidopsis. Reduced expression of OPT3 induces an over accumulation of Fe in roots and leaves, due in part by an elevated expression of the IRON‐REGULATED TRANSPORTER 1. Here we show however, that opt3 leaves display a transcriptional program consistent with an Fe overload, suggesting that Fe excess is properly sensed in opt3 leaves and that the OPT3‐mediated shoot‐to‐root signaling is critical to prevent a systemic Fe overload. We also took advantage of the tissue‐specific localization of OPT3 , together with other Fe‐responsive genes, to determine the timing and location of early transcriptional events during Fe limitation and resupply. Our results show that the leaf vasculature responds more rapidly than roots to both Fe deprivation and resupply, suggesting that the leaf vasculature is within the first tissues that sense and respond to changes in Fe availability. Our data highlight the importance of the leaf vasculature in Fe homeostasis by sensing changes in apoplastic levels of Fe coming through the xylem and relaying this information back to roots via the phloem to regulate Fe uptake at the root level.

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Research Organization:: Univ. of Missouri, Columbia, MO (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0002040; DE‐SC0002040

OSTI ID:: 1610619

Alternate ID(s):: OSTI ID: 1454889

Journal Information:: Plant, Cell and Environment, Vol. 41, Issue 10; ISSN 0140-7791

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 48 works

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References (48)

Ferritins control interaction between iron homeostasis and oxidative stress in Arabidopsis Ravet, Karl; Touraine, Brigitte; Boucherez, Jossia The Plant Journal, Vol. 57, Issue 3 https://doi.org/10.1111/j.1365-313X.2008.03698.x	journal	February 2009
The Arabidopsis AtOPT3 Protein Functions in Metal Homeostasis and Movement of Iron to Developing Seeds Stacey, Minviluz G.; Patel, Ami; McClain, William E. Plant Physiology, Vol. 146, Issue 2 https://doi.org/10.1104/pp.107.108183	journal	December 2007
Shoot to root communication is necessary to control the expression of iron-acquisition genes in Strategy I plants García, María J.; Romera, Francisco J.; Stacey, Minviluz G. Planta, Vol. 237, Issue 1 https://doi.org/10.1007/s00425-012-1757-0	journal	September 2012
The transcriptional response of Arabidopsis leaves to Fe deficiency Rodríguez-Celma, Jorge; Pan, I. Chun; Li, Wenfeng Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00276	journal	January 2013
Transcriptome Sequencing Identifies SPL7 -Regulated Copper Acquisition Genes FRO4 / FRO5 and the Copper Dependence of Iron Homeostasis in Arabidopsis Bernal, María; Casero, David; Singh, Vasantika The Plant Cell, Vol. 24, Issue 2 https://doi.org/10.1105/tpc.111.090431	journal	February 2012
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
A hitchhiker’s guide to the Arabidopsis ferrome Schmidt, Wolfgang; Buckhout, Thomas J. Plant Physiology and Biochemistry, Vol. 49, Issue 5 https://doi.org/10.1016/j.plaphy.2010.12.001	journal	May 2011
Fitting into the Harsh Reality: Regulation of Iron-deficiency Responses in Dicotyledonous Plants Ivanov, Rumen; Brumbarova, Tzvetina; Bauer, Petra Molecular Plant, Vol. 5, Issue 1 https://doi.org/10.1093/mp/ssr065	journal	January 2012
Transcriptome analysis of ein3 eil1 mutants in response to iron deficiency Bauer, Petra; Blondet, Eddy Plant Signaling & Behavior, Vol. 6, Issue 11 https://doi.org/10.4161/psb.6.11.17847	journal	November 2011
The Analysis of Arabidopsis Nicotianamine Synthase Mutants Reveals Functions for Nicotianamine in Seed Iron Loading and Iron Deficiency Responses Klatte, Marco; Schuler, Mara; Wirtz, Markus Plant Physiology, Vol. 150, Issue 1 https://doi.org/10.1104/pp.109.136374	journal	March 2009
Transcriptome analysis by GeneTrail revealed regulation of functional categories in response to alterations of iron homeostasis in Arabidopsis thaliana Schuler, Mara; Keller, Andreas; Backes, Christina BMC Plant Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2229-11-87	journal	January 2011
Iron deficiency-mediated stress regulation of four subgroup Ib BHLH genes in Arabidopsis thaliana Wang, Hong-Yu; Klatte, Marco; Jakoby, Marc Planta, Vol. 226, Issue 4 https://doi.org/10.1007/s00425-007-0535-x	journal	May 2007
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Genome Biology, Vol. 14, Issue 4 https://doi.org/10.1186/gb-2013-14-4-r36	journal	January 2013
PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis Huang, He; Yoo, Chan Yul; Bindbeutel, Rebecca eLife, Vol. 5 https://doi.org/10.7554/eLife.13292	journal	February 2016
WRKY transcription factors: Jack of many trades in plants Bakshi, Madhunita; Oelmüller, Ralf Plant Signaling & Behavior, Vol. 9, Issue 2 https://doi.org/10.4161/psb.27700	journal	February 2014
APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs Licausi, Francesco; Ohme-Takagi, Masaru; Perata, Pierdomenico New Phytologist, Vol. 199, Issue 3 https://doi.org/10.1111/nph.12291	journal	May 2013
MYB10 and MYB72 Are Required for Growth under Iron-Limiting Conditions Palmer, Christine M.; Hindt, Maria N.; Schmidt, Holger PLoS Genetics, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pgen.1003953	journal	November 2013
Dual Regulation of the Arabidopsis High-Affinity Root Iron Uptake System by Local and Long-Distance Signals Vert, Grégory A.; Briat, Jean-François; Curie, Catherine Plant Physiology, Vol. 132, Issue 2 https://doi.org/10.1104/pp.102.016089	journal	April 2003
Transporters Contributing to Iron Trafficking in Plants Conte, Sarah S.; Walker, Elsbeth L. Molecular Plant, Vol. 4, Issue 3 https://doi.org/10.1093/mp/ssr015	journal	May 2011
Phloem Ultrastructure and Pressure Flow: Sieve-Element-Occlusion-Related Agglomerations Do Not Affect Translocation Froelich, Daniel R.; Mullendore, Daniel L.; Jensen, Kåre H. The Plant Cell, Vol. 23, Issue 12 https://doi.org/10.1105/tpc.111.093179	journal	December 2011
Genetic evidence that induction of root Fe(III) chelate reductase activity is necessary for iron uptake under iron deficiency+ Yi, Ying; Guerinot, Mary Lou The Plant Journal, Vol. 10, Issue 5 https://doi.org/10.1046/j.1365-313X.1996.10050835.x	journal	November 1996
Transcriptional circuitry underlying seed coat development in Arabidopsis Khan, Deirdre; Millar, Jenna L.; Girard, Ian J. Plant Science, Vol. 219-220 https://doi.org/10.1016/j.plantsci.2014.01.004	journal	April 2014
Systems and Trans -System Level Analysis Identifies Conserved Iron Deficiency Responses in the Plant Lineage Urzica, Eugen I.; Casero, David; Yamasaki, Hiroaki The Plant Cell, Vol. 24, Issue 10 https://doi.org/10.1105/tpc.112.102491	journal	October 2012
Iron-Binding E3 Ligase Mediates Iron Response in Plants by Targeting Basic Helix-Loop-Helix Transcription Factors Selote, Devarshi; Samira, Rozalynne; Matthiadis, Anna Plant Physiology, Vol. 167, Issue 1 https://doi.org/10.1104/pp.114.250837	journal	December 2014
The bHLH Transcription Factor POPEYE Regulates Response to Iron Deficiency in Arabidopsis Roots Long, Terri A.; Tsukagoshi, Hironaka; Busch, Wolfgang The Plant Cell, Vol. 22, Issue 7 https://doi.org/10.1105/tpc.110.074096	journal	July 2010
BRUTUS and its paralogs, BTS LIKE1 and BTS LIKE2, encode important negative regulators of the iron deficiency response in Arabidopsis thaliana Hindt, Maria N.; Akmakjian, Garo Z.; Pivarski, Kara L. Metallomics, Vol. 9, Issue 7 https://doi.org/10.1039/C7MT00152E	journal	January 2017
SORTING NEXIN1 Is Required for Modulating the Trafficking and Stability of the Arabidopsis IRON-REGULATED TRANSPORTER1 Ivanov, Rumen; Brumbarova, Tzvetina; Blum, Ailisa The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.116244	journal	March 2014
OPT3 Is a Component of the Iron-Signaling Network between Leaves and Roots and Misregulation of OPT3 Leads to an Over-Accumulation of Cadmium in Seeds Mendoza-Cózatl, David G.; Xie, Qingqing; Akmakjian, Garo Z. Molecular Plant, Vol. 7, Issue 9 https://doi.org/10.1093/mp/ssu067	journal	September 2014
Nicotianamine Functions in the Phloem-Based Transport of Iron to Sink Organs, in Pollen Development and Pollen Tube Growth in Arabidopsis Schuler, Mara; Rellán-Álvarez, Rubén; Fink-Straube, Claudia The Plant Cell, Vol. 24, Issue 6 https://doi.org/10.1105/tpc.112.099077	journal	June 2012
An “Electronic Fluorescent Pictograph” Browser for Exploring and Analyzing Large-Scale Biological Data Sets Winter, Debbie; Vinegar, Ben; Nahal, Hardeep PLoS ONE, Vol. 2, Issue 8 https://doi.org/10.1371/journal.pone.0000718	journal	August 2007
Molecular mechanisms governing Arabidopsis iron uptake Brumbarova, Tzvetina; Bauer, Petra; Ivanov, Rumen Trends in Plant Science, Vol. 20, Issue 2 https://doi.org/10.1016/j.tplants.2014.11.004	journal	February 2015
Getting a sense for signals: Regulation of the plant iron deficiency response Hindt, Maria N.; Guerinot, Mary Lou Biochimica et Biophysica Acta (BBA) - Molecular Cell Research, Vol. 1823, Issue 9 https://doi.org/10.1016/j.bbamcr.2012.03.010	journal	September 2012
Iron-Induced Turnover of the Arabidopsis IRON-REGULATED TRANSPORTER1 Metal Transporter Requires Lysine Residues Kerkeb, Loubna; Mukherjee, Indrani; Chatterjee, Iera Plant Physiology, Vol. 146, Issue 4 https://doi.org/10.1104/pp.107.113282	journal	February 2008
The Diurnal Project: Diurnal and Circadian Expression Profiling, Model-based Pattern Matching, and Promoter Analysis Mockler, T. C.; Michael, T. P.; Priest, H. D. Cold Spring Harbor Symposia on Quantitative Biology, Vol. 72, Issue 1 https://doi.org/10.1101/sqb.2007.72.006	journal	January 2007
Profiling translatomes of discrete cell populations resolves altered cellular priorities during hypoxia in Arabidopsis Mustroph, A.; Zanetti, M. E.; Jang, C. J. H. Proceedings of the National Academy of Sciences, Vol. 106, Issue 44 https://doi.org/10.1073/pnas.0906131106	journal	October 2009
A Genome-Scale Resource for the Functional Characterization of Arabidopsis Transcription Factors Pruneda-Paz, Jose L.; Breton, Ghislain; Nagel, Dawn H. Cell Reports, Vol. 8, Issue 2 https://doi.org/10.1016/j.celrep.2014.06.033	journal	July 2014
Arabidopsis Yellow Stripe-Like2 (YSL2) : a metal-regulated gene encoding a plasma membrane transporter of nicotianamine-metal complexes DiDonato, Raymond J.; Roberts, Louis A.; Sanderson, Tamara The Plant Journal, Vol. 39, Issue 3 https://doi.org/10.1111/j.1365-313X.2004.02128.x	journal	August 2004
Mobilization of vacuolar iron by AtNRAMP3 and AtNRAMP4 is essential for seed germination on low iron: Iron mobilization during seed germination Lanquar, Viviane; Lelièvre, Françoise; Bolte, Susanne The EMBO Journal, Vol. 24, Issue 23 https://doi.org/10.1038/sj.emboj.7600864	journal	November 2005
OPT3 Is a Phloem-Specific Iron Transporter That Is Essential for Systemic Iron Signaling and Redistribution of Iron and Cadmium in Arabidopsis Zhai, Zhiyang; Gayomba, Sheena R.; Jung, Ha-il The Plant Cell, Vol. 26, Issue 5 https://doi.org/10.1105/tpc.114.123737	journal	May 2014
Purification of Translating Ribosomes and Associated mRNAs from Soybean ( Glycine max ) Castro‐Guerrero, Norma A.; Cui, Yaya; Mendoza‐Cozatl, David G. Current Protocols in Plant Biology, Vol. 1, Issue 1 https://doi.org/10.1002/cppb.20011	journal	May 2016
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing Benjamini, Yoav; Hochberg, Yosef Journal of the Royal Statistical Society: Series B (Methodological), Vol. 57, Issue 1 https://doi.org/10.1111/j.2517-6161.1995.tb02031.x	journal	January 1995
Plant Core Environmental Stress Response Genes Are Systemically Coordinated during Abiotic Stresses Hahn, Achim; Kilian, Joachim; Mohrholz, Anne International Journal of Molecular Sciences, Vol. 14, Issue 4 https://doi.org/10.3390/ijms14047617	journal	April 2013
The Pseudomonas fluorescens Siderophore Pyoverdine Weakens Arabidopsis thaliana Defense in Favor of Growth in Iron-Deficient Conditions Trapet, Pauline; Avoscan, Laure; Klinguer, Agnès Plant Physiology, Vol. 171, Issue 1 https://doi.org/10.1104/pp.15.01537	journal	March 2016
Feedback inhibition by thiols outranks glutathione depletion: a luciferase-based screen reveals glutathione-deficient γ-ECS and glutathione synthetase mutants impaired in cadmium-induced sulfate assimilation: Cd transcriptional response in GSH-deficient mutants Jobe, Timothy O.; Sung, Dong-Yul; Akmakjian, Garo The Plant Journal, Vol. 70, Issue 5 https://doi.org/10.1111/j.1365-313X.2012.04924.x	journal	March 2012
Expression profiling of the Arabidopsis ferric chelate reductase (FRO) gene family reveals differential regulation by iron and copper Mukherjee, Indrani; Campbell, Nathan H.; Ash, Joshua S. Planta, Vol. 223, Issue 6 https://doi.org/10.1007/s00425-005-0165-0	journal	December 2005
The analysis of arabidopsis nicotianamine synthase mutants reveals functions for nicotianamine in seed iron loading and iron deficiency responses Fink-Straube, Claudia; Klatte, Marco; Schuler, Mara Rockville, MD : American Society of Plant Biologists https://doi.org/10.34657/469	other	January 2009
TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions Kim, Daehwan; Pertea, Geo; Trapnell, Cole Springer Nature https://doi.org/10.13016/7jyb-2sdy	text	January 2013
The transcriptional response of Arabidopsis leaves to Fe deficiency Rodriguez-Celma, Jorge; Pan, I-Chun; Li, Wenfeng Humboldt-Universität zu Berlin https://doi.org/10.18452/21115	text	January 2013

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Title: Changes in iron availability in Arabidopsis are rapidly sensed in the leaf vasculature and impaired sensing leads to opposite transcriptional programs in leaves and roots

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