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BREAKTHROUGH TECHNOLOGIES

A Gateway Cloning Vector Set for High-Throughput Functional Analysis of Genes in Planta^[w]

Institute of Plant Biology and Zürich-Basel Plant Science Centre, University of Zürich, Zollikerstrasse 107, CH-8008 Zürich, Switzerland

	ABSTRACT

TOP ABSTRACT RESULTS AND DISCUSSION MATERIALS AND METHODS LITERATURE CITED

 
The current challenge, now that two plant genomes have been sequenced, is to assign a function to the increasing number of predicted genes. In Arabidopsis, approximately 55% of genes can be assigned a putative function, however, less than 8% of these have been assigned a function by direct experimental evidence. To identify these functions, many genes will have to undergo comprehensive analyses, which will include the production of chimeric transgenes for constitutive or inducible ectopic expression, for antisense or dominant negative expression, for subcellular localization studies, for promoter analysis, and for gene complementation studies. The production of such transgenes is often hampered by laborious conventional cloning technology that relies on restriction digestion and ligation. With the aim of providing tools for high throughput gene analysis, we have produced a Gateway-compatible Agrobacterium sp. binary vector system that facilitates fast and reliable DNA cloning. This collection of vectors is freely available, for noncommercial purposes, and can be used for the ectopic expression of genes either constitutively or inducibly. The vectors can be used for the expression of protein fusions to the Aequorea victoria green fluorescent protein and to the -glucuronidase protein so that the subcellular localization of a protein can be identified. They can also be used to generate promoter-reporter constructs and to facilitate efficient cloning of genomic DNA fragments for complementation experiments. All vectors were derived from pCambia T-DNA cloning vectors, with the exception of a chemically inducible vector, for Agrobacterium sp.-mediated transformation of a wide range of plant species.

Constitutive misexpression of genes, although useful in the first instance, may, however, mask tissue specific effects or may lead to lethality or sterility. To overcome these problems, several methods have been employed that control the expression temporally. Such methods include regulating gene expression using a heat shock promoter (Holtorf et al., 1995) or using a chemically induced expression system (Gatz et al., 1992; Weinmann et al., 1994; Böhner et al., 1999; Martinez et al., 1999; Bruce et al., 2000; Zuo et al., 2000). These approaches allow the activity of a gene to be studied at a specific point in the life cycle of a plant. Conversely, loss-of-function mutants can be produced using antisense constructs or dominant negative constructs and the phenotype of the plants analyzed in the absence of activity of that gene, this again may suggest its functional role. Gene expression studies that identify the expression pattern of a gene are further approaches that help elucidate gene function (Gawantka et al., 1998). In this type of analysis, evidence of the likely spatial and temporal domains of expression of a gene can be revealed. Promoter-reporter constructs are frequently used to provide supporting evidence of the functional role of genes by identifying the likely spatial and temporal domains of the expression of a gene (Batni et al., 1996; Curtis et al., 1997).

A further revealing approach to study gene function is to examine the subcellular localization of the corresponding protein. Here, studies are frequently achieved using chimeric gene fusion constructs with reporter genes. The location of the reporter protein in a subcellular compartment, as directed by the unknown fused protein, often provides additional supporting evidence for the function of the gene (von Arnim et al., 1997; Mayer et al., 1998).

Although all of these approaches are effective methods of identifying gene function, the production of the constructs is laborious and is often hampered by inappropriately positioned restriction sites that make the production of transgene constructs a "bottle neck" in plant gene functional analysis. This is particularly true when cloning large genomic DNA fragments or creating a large number of clones in a functional genomics project.

Here, we describe a complete plant vector set that aims to remove this "bottle neck," providing a reliable and effective method for the rapid directional cloning of genes and their promoters. This set of vectors is freely available for noncommercial purposes and provides a comprehensive plant molecular genetic tool kit that permits a variety of genetic manipulations from subcellular localization to inducible ectopic gene expression. These vectors facilitate high throughput DNA analysis and characterization of gene products by incorporating stop codons (in all three reading frames) adjacent to the 3' end of a Gateway (Hartley et al., 2000) cassette (where appropriate), so that genes lacking a native stop codon and flanked by att recombination sites can be freely transferred to all vectors within the series, whether the intention is to misexpress a gene or to make fusions with either -glucuronidase (GUS) or green fluorescent protein (GFP). This capability is not available in the currently described plant Gateway vectors (Karimi et al., 2002), nor is the facility to induce gene expression.

In plants, subcellular localization using GUS or GFP fusion proteins has been widely adopted to investigate protein targeting. However, often the limitations in the production of such fusion proteins has been tailoring the gene to fit the GUS or GFP fusion vector. An advantage of using this vector set is that any gene, minus its native stop codon, cloned into a donor vector (and thus flanked by attP sites) can be conservatively transferred in one step, in the correct orientation, at high efficiency, into any vector in the series that have been made in all three reading frames. A further advantage is that these vectors contain the 8-bp restriction recognition sites for AscI and PacI. These sites flank the att recombination cassettes so that positive identification of new recombination clones, in which new DNA has replaced the att recombination cassette, can be achieved efficiently.

	RESULTS AND DISCUSSION

TOP ABSTRACT RESULTS AND DISCUSSION MATERIALS AND METHODS LITERATURE CITED

 
We have constructed a variety of Gateway-compatible binary T-DNA destination vectors for a wide range of different applications in plants (Fig. 1). Details of these vectors can be found on the Web site (http://www.unizh.ch/botinst/Devo_Website/curtisvector/), which provides the complete DNA sequence and restriction maps of all constructs. The Web site will be updated by adding new constructs and relevant information, as they become available. With the exception of pMDC7, the backbone of all Gateway-compatible destination vectors is derived from the pCambia series of binary vectors for Agrobacterium sp.-mediated plant transformation (http://www.cambia.org/). The pMDC7 vector is derived from PER8 (Zuo et al., 2000). The Gateway recombination site for introduction of a DNA fragment of interest was placed towards the right border of the T-DNA in the pCambia vectors. Most of the T-DNA destination vectors described contain the hygromycin phosphotransferase plant-selectable marker gene. This selectable marker was chosen so that these vectors would be compatible with a large number of insertion lines that are kanamycin resistant, for example Ds insertions (http://genetrap.cshl.org/ and http://enhancertraps.bio.upenn.edu/EnhancerTraps.html), the SALK T-DNA insertions (http://signal.salk.edu/tabout.html), or the Arabidopsis knockout facility Madison (http://www.biotech.wisc.edu/Arabidopsis/), or that are herbicide resistant, for example SLAT lines (http://nasc.nott.ac.uk/info/slat_info1.html; Tissier et al., 1999) or the Institut National de la Recherche Agronomique lines, which are both kanamycin and herbicide resistant (http://www.Arabidopsis.org/abrc/inra.html; Bechtold et al., 1993). Vectors for complementation, however, either contain the neomycin phosphotransferase II, the hygromycin phosphotransferase, or the bialaphos acetyltransferase gene, which confer resistance to kanamycin, hygromycin, and glufosinate ammonium, respectively. All three selectable markers are under the transcriptional regulation of the cauliflower mosaic virus (CaMV) 35S promoter and nos terminator (Odell et al., 1985) and are adjacent to the left border of the T-DNA. For a comprehensive description of vector construction, refer to the supplementary materials.

View larger version (28K): [in this window] [in a new window]   Figure 1. A schematic illustrating the structure of the Gateway-compatible cloning vectors, showing the recombination sites flanked by AscI and PacI eight-nucleotide recognition sites. A, pMDC32, constitutive expression vector, harboring a dual 35S promoter, and pMDC30, a heat shock-inducible vector; B, pMDC7, derived from PER8, an estrogen-inducible vector. C, pMDC45, pMDC44, and pMDC43, for the construction of C-terminal GFP6 fusions. D, pMDC83, pMDC84, and pMDC85, for the construction of N-terminal GFP6his-tagged fusions. E, pMDC139, pMDC140, and pMDC141, for the construction of N-terminal GUS fusions. F, pMDC107, pMDC111, and pMDC110, for the construction of promoter-reporter (native promoter-gene fusion) GFP6 vectors. G, pMDC162, pMDC163, and pMDC164, for the construction of promoter-reporter (native promoter-gene fusion) GUS vectors. H, pMDC99, pMDC100, and pMDC123, for complementation of mutants with genomic fragments.

Destination Vectors for Constitutive Ectopic Gene Expression

To aid the production of constructs for the ectopic expression of genes in plants, the Gateway cassette B (see Fig. 2a) was placed adjacent to the dual 35S CaMV promoter in the destination vector pMDC32 (Fig. 1a). This promoter was chosen because it is highly active in most transgenic plant cells. The uidA gene (Jefferson et al., 1987) from an entry clone was inserted into the destination vector pMDC32 to produce an expression clone. The T₀ and T₁ generations of Arabidopsis ecotype Landsberg erecta transformed with this expression clone were tested to confirm that the Gateway-compatible construct was active in planta. These transgenic plant lines showed strong constitutive GUS activity in all of the expected plant tissue types associated with the expression of the 35S CaMV promoter (Odell et al., 1985). These plants also demonstrated that the att recombination sites do not inhibit transgene activity or interfere with enhancer activity (see supplementary data). This destination vector can, in addition to ectopic expression, be used to facilitate the rapid construction of antisense expression clones, although this latter application has not been tested.

View larger version (25K): [in this window] [in a new window]   Figure 2. Nucleotide sequence adjacent to each Gateway cassette showing the reading frame for fusions with GFP (a and b) and GUS (c). These sequences also show the stop codons in the vectors where the attR2 site is followed by the PacI site but not in vectors where the attR2 site is followed by the AscI site.

Destination Vectors for Inducible Gene Expression

Heat-Inducible Vector
Although constitutive ectopic expression of genes provides a powerful tool for gene functional studies, the resulting ubiquitous expression may lead to lethality or may mask tissue-specific effects. We therefore produced a heat shock-inducible Gateway construct. The Gateway cassette B was placed downstream of a heat shock promoter (the Gmhsp17.3B promoter fragment from the SHS3252 plasmid) in the destination vector pMDC30 (Fig. 1a). Again, the uidA gene from an entry clone was used with the pMDC30 destination vector to produce an expression clone. T₀ and T₁ generations of Arabidopsis Landsberg erecta transformants were tested to confirm that the Gateway-compatible construct was heat inducible in planta (see supplementary data). In these plants, the transgene is strongly induced in newly dividing cells, particularly in developing leaves and in the primary and lateral root tips. Control plants showed no expression in the absence of heat treatment. Heat shock induction of gene activity is an effective method of providing temporal control of ectopic transgene expression, however, the physical stress of induction at 37°C may induce the expression of other genes in the plant, masking the effects of the gene under investigation. In our hands, no obvious detrimental effects on development were observed.

Estrogen-Inducible Vector
An alternative to heat shock induction is the use of chemical induction. An estrogen-inducible ectopic gene expression vector, PER8, was described by Zuo et al. (2000). This system shows efficient induction with no toxic effects in transgenic plants. The PER8 vector was kindly provided to us by Prof. Nam-Hai Chua and was made Gateway compatible using cassette B, to produce the destination vector pMDC7 (Fig. 1b). The uidA reporter gene was inserted down-stream of the lexA-binding domain and used to transform Arabidopsis Landsberg erecta plants. T₀, T₁, and T₂ generation transformants were tested to confirm that the att recombination sites did not inhibit the estradiol-inducible expression of the reporter gene in vivo (see supplementary data). In these plants, the transgene is strongly induced ubiquitously, particularly in the roots, which were in direct contact with the inducer in the media. Control plants showed no expression in the absence of estradiol treatment.

The WUSCHEL cDNA was used to confirm that a gene without its native stop codon, when inserted into these vectors, would be expressed without interference from the additional nucleotides at the 3' end that included the att recombination site and vector sequence prior to an inframe stop codon. WUSCHEL was chosen in conjunction with the modified PER8 vector (pMDC7) because the expression of this gene after 17--estradiol induction was well characterized (Zuo et al., 2002). WUSCHEL cDNA was amplified from plasmid A1-A (Mayer, 1998; a gift from Thomas Laux) without its native stop codon. This amplified product was used to produce an Entry clone. The WUSCHEL cDNA was inserted downstream of the lexA-binding site in pMDC7. In this vector, the WUSCHEL cDNA relies on one of the stop codons in the vector to provide a translational stop. The gene now has 36 additional nucleotides, excluding the stop codon at its 3' end encoding 12 additional amino acids. T₁ generation Arabidopsis Landsberg erecta transformants were tested to confirm that these additional nucleotides did not change the estradiol-inducible expression of WUSCHEL in vivo that was previously described by Zuo et al. (2002; Fig. 3). In these plants, plant hormone independent somatic embryo formation was observed only in the presence of the inducer, confirming that the incorporation of these additional nucleotides and use of a stop codon within the vector sequence has no deterimental effect on this randomly selected gene. Control plants showed no expression in the absence of estradiol treatment.

View larger version (95K): [in this window] [in a new window]   Figure 3. 17--Estradiol induced WUSCHEL expression (a-c) in 31-d-old seedlings of three independent transformants showing germinating somatic embryos growing at the primary and lateral root tips. Noninduced seedlings show no somatic embryo development (data not shown). The same WUSCHEL gene from the same entry clone was used to make C- and N-terminal fusions with GFP and N-terminal fusions with GUS. d, f, and h show light microscope images, and e and g show fluorescent microscope images. e, Fluorescent microscope image of pMDC114 expression in bombarded onion epidermal cells (WUSCHEL cDNA, fused to C-terminus of GFP, in pMDC43). g, Fluorescent microscope image of pMDC116 expression in bombarded onion epidermal cells (WUSCHEL cDNA, fused to N-terminus of GFP, in pMDC84). h, Light microscope image of pMDC153 expression in bombarded epidermal onion cells (WUSCHEL cDNA, fused to N-terminus of GUS, in pMDC141). All show that the marker protein was localized to the nucleus.

Destination Vectors for Analysis of Subcellular Localization of Proteins

To investigate the subcellular localization of particular proteins, a further series of T-DNA destination vectors was constructed to allow C- or N-terminal protein fusions with GFP or GUS.

The vectors pMDC43, pMDC44, and pMDC45 were produced for GFP C-terminal fusions (Fig. 1c), and the vectors pMDC83, pMDC84, and pMDC85 were produced for N-terminal fusions (Fig. 1d). These vectors provide Gateway cassettes in three reading frames (Fig. 2, a and b). Gateway-compatible N-terminal fusions with GUS can also be produced using vectors pMDC139, pMDC140, and pMDC141 (Fig. 1e), again in the three reading frames (Fig. 2c).

To confirm that these vectors were suitable for studying subcellular localization of plant proteins, we created fusions between the WUSCHEL protein, previously shown to be nuclear targeted (Mayer et al., 1998), and the GFP6 or GUS proteins. To illustrate the versatility of these vectors, the same WUSCHEL entry clone (described above, containing the WUSCHEL gene without its native stop codon) was used to generate GFP and GUS fusions with WUSCHEL.

These vectors were used in biolistic bombardment experiments on onion epidermal cells (Varagona et al., 1992), and the subcellular localization of the fusion proteins was investigated by light (GUS) and fluorescence (GFP) microscopy. The results demonstrated that the GFP and GUS proteins were targeted to the nucleus when fused to the WUSCHEL protein (Fig. 3). Thus the att recombination sites do not interfere with the ability of WUSCHEL to direct the subcellular localization of the GUS or GFP proteins.

Promoter-Reporter (or Native Promoter-Gene Fusion) Constructs

For promoter-reporter analysis with GFP6, the vectors pMDC107, pMDC110, and pMDC111 were constructed (Fig. 1f). These constructs were produced with Gateway cassettes in all three reading frames so that, in addition to promoter analysis, GFP6-gene fusions could be constructed so that the fused product is under the transcriptional control of the native promoter of the gene. Similarly, the vectors pMDC162, pMDC163, and pMDC164 were constructed for promoter-reporter analysis with GUS. These constructs were again made in all three reading frames to facilitate GUS-gene fusions for subcellular localization studies using an appropriate gene with its native promoter (Fig. 1g). To test the function of these vectors, the 35S promoter was amplified from plasmid pCambia 3300 (data not shown) so that it was flanked by attB1 and attB2 sites. This amplified product was used to make a 35S-promoter entry clone (construct available, data not shown). The 35S-promoter entry clone was used to generate a GUS expression clone (construct available; data not shown). Plants transformed with this construct showed constitutive GUS expression in transgenic plant tissues, consistent with the expression pattern of the 35S promoter (see supplementary data).

Constructs for Complementation Analysis of Mutant Plant Lines

For complementation analysis in mutant backgrounds, the T-DNA destination vectors pMDC99, pMDC100, and pMDC123 can be used to rapidly clone large fragments. These three vectors contain the Gateway cassette C1 and differ from each other only in the plant selectable markers that they contain. Vector pMDC99 confers hygromycin resistance, pMDC100 confers kanamycin resistance, and pMDC123 confers BASTA resistance. Fragments of Arabidopsis genomic DNA, up to 12 kb, have been cloned successfully between att recombination sites (Norbert Huck, personal communication) using Escherichia coli DH5. It may be possible to clone larger fragments using bacterial strains such as Stbl2 (Invitrogen, Carlsbad, CA) that stabilize large genomic fragments.

In summary, we have produced a new set of Gateway-compatible plant expression vectors that enable efficient construction of transgenes for high throughput DNA analysis and characterization of gene products. These vectors provide a reliable method of cloning that reduces the usual multistep cloning approach to a single-step approach. This single-step approach is common to all vectors in the series so that a gene under investigation can be cloned using the same strategy into many vectors that have been designed to help elucidate gene function.

	MATERIALS AND METHODS

TOP ABSTRACT RESULTS AND DISCUSSION MATERIALS AND METHODS LITERATURE CITED

 

Plasmid Construction

Standard gene cloning methods (Sambrook and Russell, 2001) were used to make the gene constructs. Detailed description of how the vectors were constructed can be found in the online version of this article under supplementary data at http://www.plantphysiol.org.

Plant Materials, Growth Conditions, and Plant Transformation

Arabidopsis Landsberg erecta plants were used for plant transformations using the floral dip method (Clough and Bent, 1998). Plants were grown under continuous white light at 22°C on Murashige and Skoog agar (1x Murashige and Skoog salts, 3% [w/v] Suc, and 0.8% [w/v] agar). Detailed description of methods used in experiments can be found in the online version of this article under supplementary data at http://www.plantphysiol.org.

AttB Primers, PCR, and Recombination Reaction for Introduction of Sequences into pDONR207

Primers with attB1 and attB2 sequences were purchased from Invitrogen. PCRs and in vitro BP clonase recombination reactions were carried out according to the manufacturer's instructions (Invitrogen). The product of recombination reactions (BP reactions) was used to transform competent Escherichia coli, strain DH5 using heat shock.

Recombination Reactions for Introduction of Sequences into Destination Vectors

LR clonase reactions to transfer DNA fragments from entry clones to destination vectors were carried out according to the manufacturer's instructions (Invitrogen). The product of recombination reactions (LR reactions) was used to transform competent E. coli strain DH5 using heat shock.

Distribution of Materials

All the vectors described in this publication will be made freely available and will be distributed from the University of Zurich for noncommercial research purposes (http://www.unizh.ch/botinst/Devo_Website/curtisvector/).

	ACKNOWLEDGMENTS

 
We thank Nam-Hai Chua (Rockefeller University, New York) for kindly providing the vector PER8, the Center for Application of Molecular Biology to International Agriculture for the pCambia vectors, David Jackson (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY) for the plasmid pSKp-mgfp6, and Thomas Laux (University of Freiburg, Germany) for the plasmid A1-A. We thank Valeria Gagliardini, Jana Schneider, and Brigitte Gabathuler for help with sequencing and Peter Kopf for technical assistance. We also thank Rita Gross-Hardt and Siân Curtis for critical reading of the manuscript and Jean-Jacques Pittet for his expert help with processing images found in the supplementary data.

Received June 2, 2003; returned for revision June 17, 2003; accepted June 25, 2003.

	FOOTNOTES

 
www.plantphysiol.org/cgi/doi/10.1104/pp.103.027979.

^[w] The online version of this article contains Web-only data.

^* Corresponding author; e-mail mcurtis{at}botinst.unizh.ch; fax 4116348204.

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				M. C. Marti, E. Olmos, J. J. Calvete, I. Diaz, S. Barranco-Medina, J. Whelan, J. J. Lazaro, F. Sevilla, and A. Jimenez Mitochondrial and Nuclear Localization of a Novel Pea Thioredoxin: Identification of Its Mitochondrial Target Proteins Plant Physiology, June 1, 2009; 150(2): 646 - 657. [Abstract] [Full Text] [PDF]

				M. Quint, L. S. Barkawi, K.-T. Fan, J. D. Cohen, and W. M. Gray Arabidopsis IAR4 Modulates Auxin Response by Regulating Auxin Homeostasis Plant Physiology, June 1, 2009; 150(2): 748 - 758. [Abstract] [Full Text] [PDF]

				A. Rodrigues, J. Santiago, S. Rubio, A. Saez, K. S. Osmont, J. Gadea, C. S. Hardtke, and P. L. Rodriguez The Short-Rooted Phenotype of the brevis radix Mutant Partly Reflects Root Abscisic Acid Hypersensitivity Plant Physiology, April 1, 2009; 149(4): 1917 - 1928. [Abstract] [Full Text] [PDF]

				F. Lippold, D. H. Sanchez, M. Musialak, A. Schlereth, W.-R. Scheible, D. K. Hincha, and M. K. Udvardi AtMyb41 Regulates Transcriptional and Metabolic Responses to Osmotic Stress in Arabidopsis Plant Physiology, April 1, 2009; 149(4): 1761 - 1772. [Abstract] [Full Text] [PDF]

				S. A. MacFarlane and W. J. McGavin Genome activation by raspberry bushy dwarf virus coat protein J. Gen. Virol., March 1, 2009; 90(3): 747 - 753. [Abstract] [Full Text] [PDF]

				D. H. Chitwood, F. T.S. Nogueira, M. D. Howell, T. A. Montgomery, J. C. Carrington, and M. C.P. Timmermans Pattern formation via small RNA mobility Genes & Dev., March 1, 2009; 23(5): 549 - 554. [Abstract] [Full Text] [PDF]

				S. Schelbert, S. Aubry, B. Burla, B. Agne, F. Kessler, K. Krupinska, and S. Hortensteiner Pheophytin Pheophorbide Hydrolase (Pheophytinase) Is Involved in Chlorophyll Breakdown during Leaf Senescence in Arabidopsis PLANT CELL, March 1, 2009; 21(3): 767 - 785. [Abstract] [Full Text] [PDF]

				P. Ruggenthaler, D. Fichtenbauer, J. Krasensky, C. Jonak, and E. Waigmann Microtubule-Associated Protein AtMPB2C Plays a Role in Organization of Cortical Microtubules, Stomata Patterning, and Tobamovirus Infectivity Plant Physiology, March 1, 2009; 149(3): 1354 - 1365. [Abstract] [Full Text] [PDF]

				M. Zourelidou, I. Muller, B. C. Willige, C. Nill, Y. Jikumaru, H. Li, and C. Schwechheimer The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana Development, February 15, 2009; 136(4): 627 - 636. [Abstract] [Full Text] [PDF]

				A. Jamai, P. A. Salome, S. H. Schilling, A. P.M. Weber, and C. R. McClung Arabidopsis Photorespiratory Serine Hydroxymethyltransferase Activity Requires the Mitochondrial Accumulation of Ferredoxin-Dependent Glutamate Synthase PLANT CELL, February 1, 2009; 21(2): 595 - 606. [Abstract] [Full Text] [PDF]

				A. J. Book, J. Smalle, K.-H. Lee, P. Yang, J. M. Walker, S. Casper, J. H. Holmes, L. A. Russo, Z. W. Buzzinotti, P. D. Jenik, et al. The RPN5 Subunit of the 26s Proteasome Is Essential for Gametogenesis, Sporophyte Development, and Complex Assembly in Arabidopsis PLANT CELL, February 1, 2009; 21(2): 460 - 478. [Abstract] [Full Text] [PDF]

				M. Morel, J. Crouzet, A. Gravot, P. Auroy, N. Leonhardt, A. Vavasseur, and P. Richaud AtHMA3, a P1B-ATPase Allowing Cd/Zn/Co/Pb Vacuolar Storage in Arabidopsis Plant Physiology, February 1, 2009; 149(2): 894 - 904. [Abstract] [Full Text] [PDF]

				R. J. Schmitz, Y. Tamada, M. R. Doyle, X. Zhang, and R. M. Amasino Histone H2B Deubiquitination Is Required for Transcriptional Activation of FLOWERING LOCUS C and for Proper Control of Flowering in Arabidopsis Plant Physiology, February 1, 2009; 149(2): 1196 - 1204. [Abstract] [Full Text] [PDF]

				T. Kamiya, M. Tanaka, N. Mitani, J. F. Ma, M. Maeshima, and T. Fujiwara NIP1;1, an Aquaporin Homolog, Determines the Arsenite Sensitivity of Arabidopsis thaliana J. Biol. Chem., January 23, 2009; 284(4): 2114 - 2120. [Abstract] [Full Text] [PDF]

				A. Yilmaz, M. Y. Nishiyama Jr., B. G. Fuentes, G. M. Souza, D. Janies, J. Gray, and E. Grotewold GRASSIUS: A Platform for Comparative Regulatory Genomics across the Grasses Plant Physiology, January 1, 2009; 149(1): 171 - 180. [Abstract] [Full Text] [PDF]

				O. Berkowitz, R. Jost, S. Pollmann, and J. Masle Characterization of TCTP, the Translationally Controlled Tumor Protein, from Arabidopsis thaliana PLANT CELL, December 1, 2008; 20(12): 3430 - 3447. [Abstract] [Full Text] [PDF]

				A. P. Smertenko, D. Kaloriti, H.-Y. Chang, J. Fiserova, Z. Opatrny, and P. J. Hussey The C-Terminal Variable Region Specifies the Dynamic Properties of Arabidopsis Microtubule-Associated Protein MAP65 Isotypes PLANT CELL, December 1, 2008; 20(12): 3346 - 3358. [Abstract] [Full Text] [PDF]

				D. Xing, H. Zhao, and Q. Q. Li Arabidopsis CLP1-SIMILAR PROTEIN3, an Ortholog of Human Polyadenylation Factor CLP1, Functions in Gametophyte, Embryo, and Postembryonic Development Plant Physiology, December 1, 2008; 148(4): 2059 - 2069. [Abstract] [Full Text] [PDF]

				S. Yang, N. Johnston, E. Talideh, S. Mitchell, C. Jeffree, J. Goodrich, and G. Ingram The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development Development, November 1, 2008; 135(21): 3501 - 3509. [Abstract] [Full Text] [PDF]

				A. Saez, A. Rodrigues, J. Santiago, S. Rubio, and P. L. Rodriguez HAB1-SWI3B Interaction Reveals a Link between Abscisic Acid Signaling and Putative SWI/SNF Chromatin-Remodeling Complexes in Arabidopsis PLANT CELL, November 1, 2008; 20(11): 2972 - 2988. [Abstract] [Full Text] [PDF]

				M. Tanaka, I. S. Wallace, J. Takano, D. M. Roberts, and T. Fujiwara NIP6;1 Is a Boric Acid Channel for Preferential Transport of Boron to Growing Shoot Tissues in Arabidopsis PLANT CELL, October 1, 2008; 20(10): 2860 - 2875. [Abstract] [Full Text] [PDF]

				T. W. J. M. Van Herpen, M. Riley, C. Sparks, H. D. Jones, C. Gritsch, E. H. Dekking, R. J. Hamer, D. Bosch, E. M. J. Salentijn, M. J. M. Smulders, et al. Detailed Analysis of the Expression of an Alpha-gliadin Promoter and the Deposition of Alpha-gliadin Protein During Wheat Grain Development Ann. Bot., September 1, 2008; 102(3): 331 - 342. [Abstract] [Full Text] [PDF]

				B. S. Zheng, E. Ronnberg, L. Viitanen, T. A. Salminen, K. Lundgren, T. Moritz, and J. Edqvist Arabidopsis sterol carrier protein-2 is required for normal development of seeds and seedlings J. Exp. Bot., September 1, 2008; 59(12): 3485 - 3499. [Abstract] [Full Text] [PDF]

				P. Pedas, C. K. Ytting, A. T. Fuglsang, T. P. Jahn, J. K. Schjoerring, and S. Husted Manganese Efficiency in Barley: Identification and Characterization of the Metal Ion Transporter HvIRT1 Plant Physiology, September 1, 2008; 148(1): 455 - 466. [Abstract] [Full Text] [PDF]

				S. Rubio, L. Whitehead, T. R. Larson, I. A. Graham, and P. L. Rodriguez The Coenzyme A Biosynthetic Enzyme Phosphopantetheine Adenylyltransferase Plays a Crucial Role in Plant Growth, Salt/Osmotic Stress Resistance, and Seed Lipid Storage Plant Physiology, September 1, 2008; 148(1): 546 - 556. [Abstract] [Full Text] [PDF]

				S. Fujiwara, L. Wang, L. Han, S.-S. Suh, P. A. Salome, C. R. McClung, and D. E. Somers Post-translational Regulation of the Arabidopsis Circadian Clock through Selective Proteolysis and Phosphorylation of Pseudo-response Regulator Proteins J. Biol. Chem., August 22, 2008; 283(34): 23073 - 23083. [Abstract] [Full Text] [PDF]

				D. Kurihara, S. Matsunaga, S. Uchiyama, and K. Fukui Live Cell Imaging Reveals Plant Aurora Kinase Has Dual Roles During Mitosis Plant Cell Physiol., August 1, 2008; 49(8): 1256 - 1261. [Abstract] [Full Text] [PDF]

				L. Muniz, E. G. Minguet, S. K. Singh, E. Pesquet, F. Vera-Sirera, C. L. Moreau-Courtois, J. Carbonell, M. A. Blazquez, and H. Tuominen ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death Development, August 1, 2008; 135(15): 2573 - 2582. [Abstract] [Full Text] [PDF]

				M. Alandete-Saez, M. Ron, and S. McCormick GEX3, Expressed in the Male Gametophyte and in the Egg Cell of Arabidopsis thaliana, Is Essential for Micropylar Pollen Tube Guidance and Plays a Role during Early Embryogenesis Mol Plant, July 1, 2008; 1(4): 586 - 598. [Abstract] [Full Text] [PDF]

				M. Chen, J. E. Markham, C. R. Dietrich, J. G. Jaworski, and E. B. Cahoon Sphingolipid Long-Chain Base Hydroxylation Is Important for Growth and Regulation of Sphingolipid Content and Composition in Arabidopsis PLANT CELL, July 1, 2008; 20(7): 1862 - 1878. [Abstract] [Full Text] [PDF]

				H. Zhang, K. Ohyama, J. Boudet, Z. Chen, J. Yang, M. Zhang, T. Muranaka, C. Maurel, J.-K. Zhu, and Z. Gong Dolichol Biosynthesis and Its Effects on the Unfolded Protein Response and Abiotic Stress Resistance in Arabidopsis PLANT CELL, July 1, 2008; 20(7): 1879 - 1898. [Abstract] [Full Text] [PDF]

				I. A. Sparkes, N. A. Teanby, and C. Hawes Truncated myosin XI tail fusions inhibit peroxisome, Golgi, and mitochondrial movement in tobacco leaf epidermal cells: a genetic tool for the next generation J. Exp. Bot., June 1, 2008; 59(9): 2499 - 2512. [Abstract] [Full Text] [PDF]

				R. Hofer, I. Briesen, M. Beck, F. Pinot, L. Schreiber, and R. Franke The Arabidopsis cytochrome P450 CYP86A1 encodes a fatty acid {omega}-hydroxylase involved in suberin monomer biosynthesis J. Exp. Bot., June 1, 2008; 59(9): 2347 - 2360. [Abstract] [Full Text] [PDF]

				A. B. Sivitz, A. Reinders, and J. M. Ward Arabidopsis Sucrose Transporter AtSUC1 Is Important for Pollen Germination and Sucrose-Induced Anthocyanin Accumulation Plant Physiology, May 1, 2008; 147(1): 92 - 100. [Abstract] [Full Text] [PDF]

				W. Tang, Z. Deng, J. A. Oses-Prieto, N. Suzuki, S. Zhu, X. Zhang, A. L. Burlingame, and Z.-Y. Wang Proteomics Studies of Brassinosteroid Signal Transduction Using Prefractionation and Two-dimensional DIGE Mol. Cell. Proteomics, April 1, 2008; 7(4): 728 - 738. [Abstract] [Full Text] [PDF]

				V. Pinon, J. P. Etchells, P. Rossignol, S. A. Collier, J. M. Arroyo, R. A. Martienssen, and M. E. Byrne Three PIGGYBACK genes that specifically influence leaf patterning encode ribosomal proteins Development, April 1, 2008; 135(7): 1315 - 1324. [Abstract] [Full Text] [PDF]

				E. Magnani and S. Hake KNOX Lost the OX: The Arabidopsis KNATM Gene Defines a Novel Class of KNOX Transcriptional Regulators Missing the Homeodomain PLANT CELL, April 1, 2008; 20(4): 875 - 887. [Abstract] [Full Text] [PDF]

				N. Prunet, P. Morel, A.-M. Thierry, Y. Eshed, J. L. Bowman, I. Negrutiu, and C. Trehin REBELOTE, SQUINT, and ULTRAPETALA1 Function Redundantly in the Temporal Regulation of Floral Meristem Termination in Arabidopsis thaliana PLANT CELL, April 1, 2008; 20(4): 901 - 919. [Abstract] [Full Text] [PDF]

				C. Grefen, K. Stadele, K. Ruzicka, P. Obrdlik, K. Harter, and J. Horak Subcellular Localization and In Vivo Interactions of the Arabidopsis thaliana Ethylene Receptor Family Members Mol Plant, March 1, 2008; 1(2): 308 - 320. [Abstract] [Full Text] [PDF]

				L. R. Poulsen, R. L. Lopez-Marques, S. C. McDowell, J. Okkeri, D. Licht, A. Schulz, T. Pomorski, J. F. Harper, and M. G. Palmgren The Arabidopsis P4-ATPase ALA3 Localizes to the Golgi and Requires a {beta}-Subunit to Function in Lipid Translocation and Secretory Vesicle Formation PLANT CELL, March 1, 2008; 20(3): 658 - 676. [Abstract] [Full Text] [PDF]

				V. V. Peremyslov, A. I. Prokhnevsky, D. Avisar, and V. V. Dolja Two Class XI Myosins Function in Organelle Trafficking and Root Hair Development in Arabidopsis Plant Physiology, March 1, 2008; 146(3): 1109 - 1116. [Abstract] [Full Text] [PDF]

				S. Cai and C. C. Lashbrook Stamen Abscission Zone Transcriptome Profiling Reveals New Candidates for Abscission Control: Enhanced Retention of Floral Organs in Transgenic Plants Overexpressing Arabidopsis ZINC FINGER PROTEIN2 Plant Physiology, March 1, 2008; 146(3): 1305 - 1321. [Abstract] [Full Text] [PDF]

				R. Jonczyk, H. Schmidt, A. Osterrieder, A. Fiesselmann, K. Schullehner, M. Haslbeck, D. Sicker, D. Hofmann, N. Yalpani, C. Simmons, et al. Elucidation of the Final Reactions of DIMBOA-Glucoside Biosynthesis in Maize: Characterization of Bx6 and Bx7 Plant Physiology, March 1, 2008; 146(3): 1053 - 1063. [Abstract] [Full Text] [PDF]

				L.-Y. Lee and S. B. Gelvin T-DNA Binary Vectors and Systems Plant Physiology, February 1, 2008; 146(2): 325 - 332. [Full Text] [PDF]

				Y. Wang, D. Secco, and Y. Poirier Characterization of the PHO1 Gene Family and the Responses to Phosphate Deficiency of Physcomitrella patens Plant Physiology, February 1, 2008; 146(2): 646 - 656. [Abstract] [Full Text] [PDF]

				R. F. Mills, M. L. Doherty, R. L. Lopez-Marques, T. Weimar, P. Dupree, M. G. Palmgren, J. K. Pittman, and L. E. Williams ECA3, a Golgi-Localized P2A-Type ATPase, Plays a Crucial Role in Manganese Nutrition in Arabidopsis Plant Physiology, January 1, 2008; 146(1): 116 - 128. [Abstract] [Full Text] [PDF]

				V. Kirik, U. Herrmann, C. Parupalli, J. C. Sedbrook, D. W. Ehrhardt, and M. Hulskamp CLASP localizes in two discrete patterns on cortical microtubules and is required for cell morphogenesis and cell division in Arabidopsis J. Cell Sci., December 15, 2007; 120(24): 4416 - 4425. [Abstract] [Full Text] [PDF]

				A. Miya, P. Albert, T. Shinya, Y. Desaki, K. Ichimura, K. Shirasu, Y. Narusaka, N. Kawakami, H. Kaku, and N. Shibuya CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis PNAS, December 4, 2007; 104(49): 19613 - 19618. [Abstract] [Full Text] [PDF]

				T. Tzfira, S. V. Kozlovsky, and V. Citovsky Advanced Expression Vector Systems: New Weapons for Plant Research and Biotechnology Plant Physiology, December 1, 2007; 145(4): 1087 - 1089. [Full Text] [PDF]

				M. M. Goodin, R. Chakrabarty, R. Banerjee, S. Yelton, and S. DeBolt New Gateways to Discovery Plant Physiology, December 1, 2007; 145(4): 1100 - 1109. [Full Text] [PDF]

				M. Dafny-Yelin and T. Tzfira Delivery of Multiple Transgenes to Plant Cells Plant Physiology, December 1, 2007; 145(4): 1118 - 1128. [Full Text] [PDF]

				M. Karimi, A. Depicker, and P. Hilson Recombinational Cloning with Plant Gateway Vectors Plant Physiology, December 1, 2007; 145(4): 1144 - 1154. [Full Text] [PDF]

				M. Latijnhouwers, T. Gillespie, P. Boevink, V. Kriechbaumer, C. Hawes, and C. M. Carvalho Localization and domain characterization of Arabidopsis golgin candidates J. Exp. Bot., December 1, 2007; 58(15-16): 4373 - 4386. [Abstract] [Full Text] [PDF]

				M. Karimi, A. Bleys, R. Vanderhaeghen, and P. Hilson Building Blocks for Plant Gene Assembly Plant Physiology, December 1, 2007; 145(4): 1183 - 1191. [Abstract] [Full Text] [PDF]

				A. Himmelbach, U. Zierold, G. Hensel, J. Riechen, D. Douchkov, P. Schweizer, and J. Kumlehn A Set of Modular Binary Vectors for Transformation of Cereals Plant Physiology, December 1, 2007; 145(4): 1192 - 1200. [Abstract] [Full Text] [PDF]

				A. Para, E. M. Farre, T. Imaizumi, J. L. Pruneda-Paz, F. G. Harmon, and S. A. Kay PRR3 Is a Vascular Regulator of TOC1 Stability in the Arabidopsis Circadian Clock PLANT CELL, November 1, 2007; 19(11): 3462 - 3473. [Abstract] [Full Text] [PDF]

				N. Uchida, B. Townsley, K.-H. Chung, and N. Sinha Regulation of SHOOT MERISTEMLESS genes via an upstream-conserved noncoding sequence coordinates leaf development PNAS, October 2, 2007; 104(40): 15953 - 15958. [Abstract] [Full Text] [PDF]

				N. Winter, G. Kollwig, S. Zhang, and F. Kragler MPB2C, a Microtubule-Associated Protein, Regulates Non-Cell-Autonomy of the Homeodomain Protein KNOTTED1 PLANT CELL, October 1, 2007; 19(10): 3001 - 3018. [Abstract] [Full Text] [PDF]

				Y. Tsegaye, C. G. Richardson, J. E. Bravo, B. J. Mulcahy, D. V. Lynch, J. E. Markham, J. G. Jaworski, M. Chen, E. B. Cahoon, and T. M. Dunn Arabidopsis Mutants Lacking Long Chain Base Phosphate Lyase Are Fumonisin-sensitive and Accumulate Trihydroxy-18:1 Long Chain Base Phosphate J. Biol. Chem., September 21, 2007; 282(38): 28195 - 28206. [Abstract] [Full Text] [PDF]

				F. Li, T. Asami, X. Wu, E. W.T. Tsang, and A. J. Cutler A Putative Hydroxysteroid Dehydrogenase Involved in Regulating Plant Growth and Development Plant Physiology, September 1, 2007; 145(1): 87 - 97. [Abstract] [Full Text] [PDF]

				S. A. Saracco, M. J. Miller, J. Kurepa, and R. D. Vierstra Genetic Analysis of SUMOylation in Arabidopsis: Conjugation of SUMO1 and SUMO2 to Nuclear Proteins Is Essential Plant Physiology, September 1, 2007; 145(1): 119 - 134. [Abstract] [Full Text] [PDF]

				Y. Nakagawa, H. Hanaoka, M. Kobayashi, K. Miyoshi, K. Miwa, and T. Fujiwara Cell-Type Specificity of the Expression of Os BOR1, a Rice Efflux Boron Transporter Gene, Is Regulated in Response to Boron Availability for Efficient Boron Uptake and Xylem Loading PLANT CELL, August 1, 2007; 19(8): 2624 - 2635. [Abstract] [Full Text] [PDF]

				Y. Yan, S. Stolz, A. Chetelat, P. Reymond, M. Pagni, L. Dubugnon, and E. E. Farmer A Downstream Mediator in the Growth Repression Limb of the Jasmonate Pathway PLANT CELL, August 1, 2007; 19(8): 2470 - 2483. [Abstract] [Full Text] [PDF]

				M. N. Martin, P. H. Saladores, E. Lambert, A. O. Hudson, and T. Leustek Localization of Members of the {gamma}-Glutamyl Transpeptidase Family Identifies Sites of Glutathione and Glutathione S-Conjugate Hydrolysis Plant Physiology, August 1, 2007; 144(4): 1715 - 1732. [Abstract] [Full Text] [PDF]

				C. Lunde, D. P. Drew, A. K. Jacobs, and M. Tester Exclusion of Na+ via Sodium ATPase (PpENA1) Ensures Normal Growth of Physcomitrella patens under Moderate Salt Stress Plant Physiology, August 1, 2007; 144(4): 1786 - 1796. [Abstract] [Full Text] [PDF]

				K. Kobayashi, M. S. Otegui, S. Krishnakumar, M. Mindrinos, and P. Zambryski INCREASED SIZE EXCLUSION LIMIT2 Encodes a Putative DEVH Box RNA Helicase Involved in Plasmodesmata Function during Arabidopsis Embryogenesis PLANT CELL, June 1, 2007; 19(6): 1885 - 1897. [Abstract] [Full Text] [PDF]

				K. Marinova, L. Pourcel, B. Weder, M. Schwarz, D. Barron, J.-M. Routaboul, I. Debeaujon, and M. Klein The Arabidopsis MATE Transporter TT12 Acts as a Vacuolar Flavonoid/H+-Antiporter Active in Proanthocyanidin-Accumulating Cells of the Seed Coat PLANT CELL, June 1, 2007; 19(6): 2023 - 2038. [Abstract] [Full Text] [PDF]

				P. A. Reeves, Y. He, R. J. Schmitz, R. M. Amasino, L. W. Panella, and C. M. Richards Evolutionary Conservation of the FLOWERING LOCUS C-Mediated Vernalization Response: Evidence From the Sugar Beet (Beta vulgaris) Genetics, May 1, 2007; 176(1): 295 - 307. [Abstract] [Full Text] [PDF]

				F. Chopin, M. Orsel, M.-F. Dorbe, F. Chardon, H.-N. Truong, A. J. Miller, A. Krapp, and F. Daniel-Vedele The Arabidopsis ATNRT2.7 Nitrate Transporter Controls Nitrate Content in Seeds PLANT CELL, May 1, 2007; 19(5): 1590 - 1602. [Abstract] [Full Text] [PDF]

				J. F. Uhrig, M. Mutondo, I. Zimmermann, M. J. Deeks, L. M. Machesky, P. Thomas, S. Uhrig, C. Rambke, P. J. Hussey, and M. Hulskamp The role of Arabidopsis SCAR genes in ARP2-ARP3-dependent cell morphogenesis Development, March 1, 2007; 134(5): 967 - 977. [Abstract] [Full Text] [PDF]

				S. Yehudai-Resheff, S. L. Zimmer, Y. Komine, and D. B. Stern Integration of Chloroplast Nucleic Acid Metabolism into the Phosphate Deprivation Response in Chlamydomonas reinhardtii PLANT CELL, March 1, 2007; 19(3): 1023 - 1038. [Abstract] [Full Text] [PDF]

				Q. Zeng, X. Wang, and M. P. Running Dual Lipid Modification of Arabidopsis G{gamma}-Subunits Is Required for Efficient Plasma Membrane Targeting Plant Physiology, March 1, 2007; 143(3): 1119 - 1131. [Abstract] [Full Text] [PDF]

				A. B. Sivitz, A. Reinders, M. E. Johnson, A. D. Krentz, C. P.L. Grof, J. M. Perroux, and J. M. Ward Arabidopsis Sucrose Transporter AtSUC9. High-Affinity Transport Activity, Intragenic Control of Expression, and Early Flowering Mutant Phenotype Plant Physiology, January 1, 2007; 143(1): 188 - 198. [Abstract] [Full Text] [PDF]

				M. Chen, G. Han, C. R. Dietrich, T. M. Dunn, and E. B. Cahoon The Essential Nature of Sphingolipids in Plants as Revealed by the Functional Identification and Characterization of the Arabidopsis LCB1 Subunit of Serine Palmitoyltransferase PLANT CELL, December 1, 2006; 18(12): 3576 - 3593. [Abstract] [Full Text] [PDF]

				S. Goepfert, J. K. Hiltunen, and Y. Poirier Identification and Functional Characterization of a Monofunctional Peroxisomal Enoyl-CoA Hydratase 2 That Participates in the Degradation of Even cis-Unsaturated Fatty Acids in Arabidopsis thaliana J. Biol. Chem., November 24, 2006; 281(47): 35894 - 35903. [Abstract] [Full Text] [PDF]

				M. E. Salvucci, B. P. DeRidder, and A. R. Portis Jr Effect of activase level and isoform on the thermotolerance of photosynthesis in Arabidopsis J. Exp. Bot., November 1, 2006; 57(14): 3793 - 3799. [Abstract] [Full Text] [PDF]

				N. Basherudin and M. D. Curtis Identification of Positive GATEWAY Expression Clones When Both the pENTRY and pDEST Vectors Contain the Same Marker for Bacterial Selection CSH Protocols, November 1, 2006; 2006(29): pdb.prot4647 - pdb.prot4647. [Abstract] [Full Text]

				K. Ohashi-Ito and D. C. Bergmann Arabidopsis FAMA Controls the Final Proliferation/Differentiation Switch during Stomatal Development PLANT CELL, October 1, 2006; 18(10): 2493 - 2505. [Abstract] [Full Text] [PDF]

				Y.-S. Wang, R. Shrestha, A. Kilaru, W. Wiant, B. J. Venables, K. D. Chapman, and E. B. Blancaflor Manipulation of Arabidopsis fatty acid amide hydrolase expression modifies plant growth and sensitivity to N-acylethanolamines PNAS, August 8, 2006; 103(32): 12197 - 12202. [Abstract] [Full Text] [PDF]

				L. Brand, M. Horler, E. Nuesch, S. Vassalli, P. Barrell, W. Yang, R. A. Jefferson, U. Grossniklaus, and M. D. Curtis A Versatile and Reliable Two-Component System for Tissue-Specific Gene Induction in Arabidopsis Plant Physiology, August 1, 2006; 141(4): 1194 - 1204. [Abstract] [Full Text] [PDF]

				R. Bari, B. Datt Pant, M. Stitt, and W.-R. Scheible PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants Plant Physiology, July 1, 2006; 141(3): 988 - 999. [Abstract] [Full Text] [PDF]

				K. Aung, S.-I Lin, C.-C. Wu, Y.-T. Huang, C.-l. Su, and T.-J. Chiou pho2, a Phosphate Overaccumulator, Is Caused by a Nonsense Mutation in a MicroRNA399 Target Gene Plant Physiology, July 1, 2006; 141(3): 1000 - 1011. [Abstract] [Full Text] [PDF]

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