Transposon-Mediated Alteration of TaMATE1B Expression in Wheat Confers Constitutive Citrate Efflux from Root Apices[W]

Summary: This research describes how a mobile genetic element recruits the TaMATE1B gene into a role associated with aluminum tolerance by altering its expression level and pattern. The TaMATE1B gene (for multidrug and toxic compound extrusion) from wheat (Triticum aestivum) was isolated and shown to encode a citrate transporter that is located on the plasma membrane. TaMATE1B expression in roots was induced by iron deficiency but not by phosphorus deficiency or aluminum treatment. The coding region of TaMATE1B was identical in a genotype showing citrate efflux from root apices (cv Carazinho) to one that lacked citrate efflux (cv Egret). However, sequence upstream of the coding region differed between these two genotypes in two ways. The first difference was a single-nucleotide polymorphism located approximately 2 kb upstream from the start codon in cv Egret. The second difference was an 11.1-kb transposon-like element located 25 bp upstream of the start codon in cv Carazinho that was absent from cv Egret. The influence of these polymorphisms on TaMATE1B expression was investigated using fusions to green fluorescent protein expressed in transgenic lines of rice (Oryza sativa). Fluorescence measurements in roots of rice indicated that 1.5- and 2.3-kb regions upstream of TaMATE1B in cv Carazinho (which incorporated 3′ regions of the transposon-like element) generated 20-fold greater expression in the apical 1 mm of root compared with the native promoter in cv Egret. By contrast, fluorescence in more mature tissues was similar in both cultivars. The presence of the single-nucleotide polymorphism alone consistently generated 2-fold greater fluorescence than the cv Egret promoter. We conclude that the transposon-like element in cv Carazinho extends TaMATE1B expression to the root apex, where it confers citrate efflux and enhanced aluminum tolerance.

[1]  Rainer Hedrich,et al.  AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. , 2010, The Plant journal : for cell and molecular biology.

[2]  E. Delhaize,et al.  FUNCTION AND MECHANISM OF ORGANIC ANION EXUDATION FROM PLANT ROOTS. , 2001, Annual review of plant physiology and plant molecular biology.

[3]  Ofer Peleg,et al.  Large Retrotransposon Derivatives: Abundant, Conserved but Nonautonomous Retroelements of Barley and Related Genomes , 2004, Genetics.

[4]  H. Murer,et al.  Voltage Clamp Fluorometric Measurements on a Type II Na+-coupled Pi Cotransporter: Shedding Light on Substrate Binding Order , 2006, The Journal of general physiology.

[5]  Keyan Zhao,et al.  Genetic Architecture of Aluminum Tolerance in Rice (Oryza sativa) Determined through Genome-Wide Association Analysis and QTL Mapping , 2011, PLoS genetics.

[6]  E. Delhaize,et al.  Transcriptional regulation of aluminium tolerance genes. , 2012, Trends in plant science.

[7]  T. Furuichi,et al.  Closing Plant Stomata Requires a Homolog of an Aluminum-Activated Malate Transporter , 2010, Plant & cell physiology.

[8]  E. Delhaize,et al.  Aluminum Tolerance in Wheat (Triticum aestivum L.) (II. Aluminum-Stimulated Excretion of Malic Acid from Root Apices) , 1993, Plant physiology.

[9]  L. Kochian,et al.  Novel Properties of the Wheat Aluminum Tolerance Organic Acid Transporter (TaALMT1) Revealed by Electrophysiological Characterization in Xenopus Oocytes: Functional and Structural Implications1[OA] , 2008, Plant Physiology.

[10]  K. Takeda,et al.  An aluminum-activated citrate transporter in barley. , 2007, Plant & cell physiology.

[11]  N. Yamaji,et al.  OsFRDL 1 Is a Citrate Transporter Required for Efficient Translocation of Iron in Rice 1 [ OA ] , 2008 .

[12]  L. Kochian,et al.  Aluminum-activated citrate and malate transporters from the MATE and ALMT families function independently to confer Arabidopsis aluminum tolerance. , 2009, The Plant journal : for cell and molecular biology.

[13]  L. Kochian,et al.  A de novo synthesis citrate transporter, Vigna umbellata multidrug and toxic compound extrusion, implicates in Al-activated citrate efflux in rice bean (Vigna umbellata) root apex. , 2011, Plant, cell & environment.

[14]  E. Delhaize,et al.  Analysis of TaALMT1 traces the transmission of aluminum resistance in cultivated common wheat (Triticum aestivum L.) , 2008, Theoretical and Applied Genetics.

[15]  G. Bai,et al.  Quantitative trait loci for aluminum resistance in wheat , 2007, Molecular Breeding.

[16]  Michele Morgante,et al.  Transposable elements and the plant pan-genomes. , 2007, Current opinion in plant biology.

[17]  L. Kochian,et al.  Two functionally distinct members of the MATE (multi-drug and toxic compound extrusion) family of transporters potentially underlie two major aluminum tolerance QTLs in maize. , 2010, The Plant journal : for cell and molecular biology.

[18]  P. Waterhouse,et al.  A suite of novel promoters and terminators for plant biotechnology. II. The pPLEX series for use in monocots. , 2003, Functional plant biology : FPB.

[19]  S. Oka,et al.  Early infection of scutellum tissue with Agrobacterium allows high-speed transformation of rice. , 2006, The Plant journal : for cell and molecular biology.

[20]  B. Gunning,et al.  A plasmolytic cycle: The fate of cytoskeletal elements , 2000, Protoplasma.

[21]  K. Takeda,et al.  Molecular mapping of a gene responsible for Al-activated secretion of citrate in barley. , 2004, Journal of experimental botany.

[22]  Sung-ju Ahn,et al.  A wheat gene encoding an aluminum-activated malate transporter. , 2004, The Plant journal : for cell and molecular biology.

[23]  Milton H Saier,et al.  The multidrug/oligosaccharidyl-lipid/polysaccharide (MOP) exporter superfamily. , 2003, European journal of biochemistry.

[24]  E. Delhaize,et al.  A Second Mechanism for Aluminum Resistance in Wheat Relies on the Constitutive Efflux of Citrate from Roots1[W][OA] , 2008, Plant Physiology.

[25]  L. Kochian,et al.  Association and Linkage Analysis of Aluminum Tolerance Genes in Maize , 2010, PloS one.

[26]  L. Kochian,et al.  A gene in the multidrug and toxic compound extrusion (MATE) family confers aluminum tolerance in sorghum , 2007, Nature Genetics.

[27]  Kazuhiro Sato,et al.  Acquisition of aluminium tolerance by modification of a single gene in barley , 2012, Nature Communications.

[28]  C. Picco,et al.  The Arabidopsis vacuolar malate channel is a member of the ALMT family. , 2007, The Plant journal : for cell and molecular biology.

[29]  Hikmet Budak,et al.  Megabase Level Sequencing Reveals Contrasted Organization and Evolution Patterns of the Wheat Gene and Transposable Element Spaces[W] , 2010, Plant Cell.

[30]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[31]  S. Howitt,et al.  HvALMT1 from barley is involved in the transport of organic anions , 2010, Journal of experimental botany.

[32]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[33]  L. Kochian,et al.  Molecular characterization and mapping of ALMT1, the aluminium-tolerance gene of bread wheat (Triticum aestivum L.). , 2005, Genome.

[34]  E. Delhaize,et al.  Engineering high-level aluminum tolerance in barley with the ALMT1 gene. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[35]  E. Delhaize,et al.  Characterization of promoter expression patterns derived from the Pht1 phosphate transporter genes of barley (Hordeum vulgare L.). , 2004, Journal of experimental botany.

[36]  A. Green,et al.  A leaf-based assay using interchangeable design principles to rapidly assemble multistep recombinant pathways. , 2009, Plant biotechnology journal.

[37]  P. Waterhouse,et al.  A suite of novel promoters and terminators for plant biotechnology. , 2003, Functional plant biology : FPB.

[38]  J. V. Magalhaes,et al.  How a microbial drug transporter became essential for crop cultivation on acid soils: aluminium tolerance conferred by the multidrug and toxic compound extrusion (MATE) family. , 2010, Annals of botany.

[39]  E. Delhaize,et al.  Malate Efflux From Root Apices and Tolerance to Aluminium Are Highly Correlated in Wheat , 1995 .

[40]  Wen‐Hao Zhang,et al.  Characterization of the TaALMT1 protein as an Al3+-activated anion channel in transformed tobacco (Nicotiana tabacum L.) cells. , 2008, Plant & cell physiology.

[41]  F. Gage,et al.  The necessary junk: new functions for transposable elements. , 2007, Human molecular genetics.

[42]  E. Delhaize,et al.  High-resolution mapping of the Alp locus and identification of a candidate gene HvMATE controlling aluminium tolerance in barley (Hordeum vulgare L.) , 2007, Theoretical and Applied Genetics.

[43]  B. Burla,et al.  Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. , 2011, The Plant journal : for cell and molecular biology.

[44]  W. Gassmann,et al.  The FRD3-Mediated Efflux of Citrate into the Root Vasculature Is Necessary for Efficient Iron Translocation1[OA] , 2007, Plant Physiology.

[45]  E. Delhaize,et al.  The convergent evolution of aluminium resistance in plants exploits a convenient currency , 2010 .

[46]  A. Schulman,et al.  The BARE-1 retrotransposon is transcribed in barley from an LTR promoter active in transient assays , 1996, Plant Molecular Biology.

[47]  N. Yamaji,et al.  OsFRDL1 Is a Citrate Transporter Required for Efficient Translocation of Iron in Rice1[OA] , 2008, Plant Physiology.

[48]  J. Pittman,et al.  A role for the AtMTP11 gene of Arabidopsis in manganese transport and tolerance. , 2007, The Plant journal : for cell and molecular biology.

[49]  Sung-ju Ahn,et al.  Evidence for the plasma membrane localization of Al-activated malate transporter (ALMT1). , 2005, Plant & cell physiology.

[50]  T. Furuichi,et al.  The identification of aluminium-resistance genes provides opportunities for enhancing crop production on acid soils. , 2011, Journal of experimental botany.