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Update on Legume Transcription Factors

Legume Transcription Factors: Global Regulators of Plant Development and Response to the Environment^1,[W]

The Samuel Roberts Noble Foundation, Ardmore, Oklahoma 73401 (M.K.U., J.M., A.A., J.-Y.Z.,V.B.); Max Planck Institute for Molecular Plant Physiology, 14476 Potsdam-Golm, Germany (M.K.U., K.K., M.W.,O.M.); John Innes Centre, Norwich NR4 7UH, United Kingdom (J.M.I.H.); and The Institute for Genomic Research, Rockville, Maryland (F.C., C.D.T.)

Transcription factors (TFs) are DNA-binding proteins that interact with other transcriptional regulators, including chromatin remodeling/modifying proteins, to recruit or block access of RNA polymerases to the DNA template. Plant genomes devote approximately 7% of their coding sequence to TFs, which is a testament to the complexity of transcriptional regulation in these organisms. Extensive sequencing of cDNA and genomic DNA indicates that legumes encode upwards of 2,000 TFs per genome. Less than 1% of these have been characterized genetically, although TFs likely played seminal roles in legume evolution and clearly now play crucial roles in plant development and differentiation. Here we review the literature on legume TFs and describe technological developments that are paving the way for rapid and systematic characterization of TFs and the genetic regulatory networks they control.

Plants are amazing organisms. Not only are they able to build complex organic superstructures from simple inorganic molecules that ensure their growth and reproductive success, but they do this while fixed in space and subject to environmental extremes of light, temperature, water, and nutrients, and to biological challenges from competitors, pests, and pathogens. Evolution has endowed plants with a flexible developmental program that enables them to elaborate new vegetative organs and attune reproduction to prevailing environmental conditions. Plant cells can also differentiate in the short term to cope with more immediate environmental challenges. Plant development and differentiation are programmed primarily at the level of gene transcription, which is controlled by TFs and other proteins that either recruit or block access of RNA polymerases to the DNA template. TFs are usually defined as sequence-specific DNA-binding proteins that are capable of activating and/or repressing transcription. Plant genomes appear to encode many more TFs than those of animals, such as Caenorhabditis elegans and Drosophila melanogaster, which indicates that transcriptional regulation in plants is at least as complex as in animals (Riechmann et al., 2000). Arabidopsis (Arabidopsis thaliana) possesses upwards of 1,800 TF genes representing more than 7% of all protein-coding genes (Riechmann et al., 2000; Guo et al., 2005; Iida et al., 2005). Surprisingly, only one-tenth of these have been characterized genetically (Qu and Zhu, 2006) despite the enormous resources that have been devoted to Arabidopsis research over the past decade. Not surprisingly, we know far less about the role of TFs in other plant species. For instance, less than 1% of TF genes in the model legumes Lotus japonicus (or simply Lotus) and Medicago truncatula (or Medicago) have been genetically characterized. This makes review of the literature on legume TFs a relatively simple task at present, although there are signs that this situation will change rapidly over the next few years. First of all, it is already apparent that TFs play crucial roles in agriculturally important processes in legumes, such as symbiotic nitrogen fixation (SNF), so there is great incentive to learn more about this important class of regulatory proteins. Second, the genome of three legume species, Medicago, Lotus, and soybean (Glycine max), will be completed or largely so in the next 2 years, which will enable the identification of most of the TFs in these species via bioinformatics approaches. Finally, numerous tools for functional genomics have been and are being developed that will facilitate rapid and systematic functional characterization of large numbers of TFs. This review summarizes our current state of knowledge about legume TFs and considers the opportunities and challenges for continued research in this area.

	THE DYNAMIC TRANSCRIPTOME

TOP THE DYNAMIC TRANSCRIPTOME IDENTIFICATION OF PUTATIVE TFs FUNCTIONAL CHARACTERIZATION OF... A ROADMAP FOR FUTURE... LITERATURE CITED

 
As a backdrop to our discussion of legume TFs, it is salient that recent transcriptomic studies, using arrays of cDNA or oligonucleotides to measure transcript levels, have identified thousands of legume genes that are differentially expressed during various types of plant-microbe interactions (Colebatch et al., 2002, 2004; Liu et al., 2003; Barnett et al., 2004; El-Yahyaoui et al., 2004; Kouchi et al., 2004; Lee et al., 2004; Manthey et al., 2004; Mitra et al., 2004; Moy et al., 2004; Suganuma et al., 2004; Hohnjec et al., 2005; Zou et al., 2005; Alkharouf et al., 2006; Lohar et al., 2006; Starker et al., 2006; Zabala et al., 2006), development and differentiation (Vodkin et al., 2004; Aziz et al., 2005; Firnhaber et al., 2005; Dhaubhadel et al., 2007), and in response to abiotic stress (Ainsworth et al., 2006; Buitink et al., 2006). Invariably, TFs have been found among differentially expressed genes, implicating them in the regulation of specific developmental processes or responses to the biotic and abiotic environment. Such guilt by association is a theme that is elaborated upon below.

	IDENTIFICATION OF PUTATIVE TFs

TOP THE DYNAMIC TRANSCRIPTOME IDENTIFICATION OF PUTATIVE TFs FUNCTIONAL CHARACTERIZATION OF... A ROADMAP FOR FUTURE... LITERATURE CITED

 
Bioinformatics approaches have been instrumental in identifying putative TF genes in plants. TF families are generally defined by the types of DNA-binding domain contained by proteins in the family (Table I ; Fig. 1 ) and putative TF genes have been identified primarily on the basis of DNA sequences within the gene that encode known DNA-binding domains (Riechmann et al., 2000; Guo et al., 2005; Iida et al., 2005). BLAST and similar searches that look for extended sequence homology between query sequences and known TFs have also been used to identify putative TFs (Iida et al., 2005). BLAST searches that utilize well-curated protein databases, such as UniProt (http://www.expasy.uniprot.org/database/knowledgebase.shtml), can also be used to support TF annotations that were made initially on the basis of the presence of a DNA-binding or other characteristic domain. We searched the current International Medicago Gene Annotation Group (IMGAG) dataset, which contains 40,568 predicted proteins, for the presence of sequences encoding DNA-binding and other TF domains to identify putative TF genes in this species (Supplemental Table S1). A subset of these TFs, obtained from an earlier release of IMGAG gene annotations, was verified by BLAST analysis, which resulted in a list of 1,084 putative TF genes (Table I). We have designed and tested gene-specific primers for each of these for use in high-throughput quantitative reverse transcription (qRT)-PCR analysis and have plans to develop this resource further to facilitate transcript analysis of all Medicago TF genes in the future (K. Kakar and M.K. Udvardi, unpublished data).

View larger version (23K): [in this window] [in a new window] [as a PowerPoint slide]   Figure 1. Relationships and domain shuffling between Medicago TF families. TF families are represented by circles whose size is proportional to the number of members in the family. Domains are represented by rectangles, whose size is proportional to the domain length. DNA-binding domains appear in color. Protein-binding and other domains are hatched. Dashed lines indicate that a given domain is characteristic of the family or subfamily to which it is attached. Dotted lines indicate domains that define a potentially novel TF family or subfamily. Based on Figure 1 of Riechmann (2002).

	FUNCTIONAL CHARACTERIZATION OF TFs

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Whereas research to identify TFs involved in SNF has profited little from previous work in nonlegumes such as Arabidopsis, knowledge from nonlegume models has been instrumental in identifying a number of TF genes involved in common plant processes, such as flower and leaf development (Table II). In fact, the first legume TF gene to be characterized functionally was pea (Pisum sativum) FLO, which was isolated by virtue of its sequence homology to the TFs FLO and LFY of snapdragon (Antirrhinum majus) and Arabidopsis, respectively. FLO and LFY control floral development in snapdragon and Arabidopsis, and a defect in pea FLO was subsequently found to be responsible for aberrant floral and leaf development in the pea unifoliata (uni) mutant (Hofer et al., 1997). The Lotus ortholog of FLO was later identified in the same way (Dong et al., 2005). Similar approaches were used to assign functions for PIM (a MADS family TF) in pea floral meristem determination (Taylor et al., 2002) and for PHANTASTICA (a MYB TF) in pea compound leaf development (Tattersall et al., 2005). Interestingly, Lotus has a duplicate pair of PHANTASTICA-like genes that probably have divergent functions in compound leaf development (Luo et al., 2005).

The value of computational approaches in identifying genes likely to be involved in various aspects of flowering was nicely illustrated by Hecht et al. (2005), who utilized sequence information from Arabidopsis TFs to identify homologs in model legume sequence databases, which were then used to design PCR-cloning strategies to isolate homologs from pea. The majority of Arabidopsis flowering genes were represented in pea and other legume sequence databases. However, several gene families, including the MADS-box, CONSTANS, and FLOWERING LOCUS T/TERMINAL FLOWER1 families, appeared to have undergone differential expansion, whereas other genes important in Arabidopsis, including FRIGIDA and members of the FLOWERING LOCUS C clade, were conspicuously absent from legumes. Several pea and Medicago orthologs mapped to syntenic chromosomal positions, demonstrating the benefit of parallel model systems for understanding flowering phenology in crop and model legume species.

TFs of the TCP family, named after the founding members TB1, CYC, and PCF, help to establish the pattern of flower petals (Cubas, 2004), which gives legume flowers their typical bilateral symmetry. Citerne et al. (2003) sequenced a number of CYC homologs, sorted them into clades by phylogenetic analysis, and discussed the difficulties of assigning orthologs in cross-species comparisons. Thus, genetic map position, mutant phenotypes, and/or complementation of Arabidopsis mutants have been used in addition to sequence similarity to infer orthology. The squared standard mutant of Lotus is defective in the TCP gene LjCYC2, which is required to establish floral bilateral symmetry and was cloned by a candidate gene/sequence homology approach (Feng et al., 2006). Adaxial expression of two CYC genes was observed in the developing floral meristem of lupin (Lupinus albus), which also has bilaterally symmetrical flowers (Citerne et al., 2006). Interestingly, evolution of radially symmetrical flowers in Cadia, which belongs to the same subclade as Lupinus, may have resulted from an expanded domain of expression of an orthologous CYC gene in the former (Citerne et al., 2006).

Cross-species complementation studies have indicated possible roles for several legume TFs. For example, Berbel et al. (2001) rescued the Arabidopsis apetala1 (ap1) floral development mutant using a PIM cDNA clone, which they called PEAM4. Later, the same group characterized PsPI, a pea MADS-box gene homologous to the petal and stamen identity genes PISTILLATA (PI), from Arabidopsis and GLOBOSA, from snapdragon. Interestingly, constitutive expression of PsPI in Arabidopsis rescued the floral defects caused by the strong pi-1 mutant allele, despite the fact that the pea protein, PsPI, lacked a particular C-terminal motif (Berbel et al., 2005). Similarly, Guo and Gan (2006) showed that overexpression of PvNAP, a kidney bean (Phaseolus vulgaris) NAC TF homologous to Arabidopsis AtNAP, successfully complemented the leaf abscission phenotype of an atnap null mutant, indicating a possible role of NAP in bean leaf abscission.

Finally, five legume TFs have been implicated in abiotic stress tolerance (Table II). One of these, alfalfa Mszpt2-1, which was mentioned previously in the context of nodule development, was found to be induced in roots by salt treatment. Inhibition of Mszpt2-1 by antisense RNA resulted in increased sensitivity of transgenic plants to salinity (Merchan et al., 2003). Overexpression of CAP2 and Alfin1 TFs in transgenic plants conferred salt tolerance and increased growth (Winicov, 2000; Shukla et al., 2006). Constitutive overexpression of SCOF-1, a soybean protein, increased cold tolerance of transgenic Arabidopsis and tobacco (Nicotiana tabacum) plants (Kim et al., 2001). Another example of successful leveraging of knowledge from nonlegumes for legume research is provided by the Medicago WXP1 gene, a member of the AP2/ethylene-responsive element-binding protein (EREBP) family of TFs. Several members of this family have been implicated in drought tolerance in Arabidopsis and other nonlegumes. Overexpression of Medicago WXP1 in alfalfa resulted in enhanced tolerance to drought stress, which correlated with increased wax deposition in the leaf cuticle (Zhang et al., 2005).

Whereas work on deciphering the roles of legume TFs is just beginning, considerable efforts have already been made to demonstrate the functionality of such proteins in terms of their DNA-binding and transactivation abilities and subcellular localization (Table III ). Approaches for isolating legume TF genes have varied widely. Homology-based methods using TF DNA from other plant families have been successfully employed to identify specific classes of legume TFs. For instance, GmEREBP1 was isolated from a soybean root cDNA library screened with a probe that was PCR amplified using degenerate primers matching the conserved EREBP-coding domain (Mazarei et al., 2002). Three soybean DRE-binding proteins were identified by sequence homology to the AP2/EREBP consensus sequence via a BLAST search of the soybean EST database (Li et al., 2005). Several groups have used degenerate primers matching conserved TF domains for PCR amplification of legume TF sequences (Chern et al., 1996a, 1996b; Heard et al., 1997; Uimari and Strommer, 1997; Zucchero et al., 2001; Tucker et al., 2002).

Approaches to demonstrate DNA binding of legume TFs include electrophoretic mobility shift assays (EMSAs), hybridization of labeled DNA to TFs on filters, DNase-I footprinting, and yeast one-hybrid assays (Table III). In one interesting example, Bastola et al. (1998) identified cDNA encoding Alfin1, a protein with a putative Zn-binding domain, by differential screening of salt-tolerant alfalfa cells. The DNA-binding specificity of Alfin1 was determined by binding of purified protein to random oligonucleotides in an EMSA followed by PCR amplification to identify the preferential target sites. In most instances, however, DNA-binding specificity has been tested only on a few select cis-element sequences that have been identified by work in other plant families. Such biased approaches are likely to miss important TF-DNA interactions. Alternative, nonbiased approaches are now available that should solve this problem (see below).

Further evidence of TF activity has occasionally been provided using transactivation assays. Some groups have demonstrated in vivo transactivation in cell culture and transient transformation systems, including particle bombardment of bean cotyledons (Chern et al., 1996a, 1996b; Bobb et al., 1997), polyethylene glycol-mediated transfection of Arabidopsis protoplasts (Kim et al., 2001), and in vitro transcription activation in rice (Oryza sativa) cell extracts (Lindsay et al., 2002).

One verification of a protein's role as a TF is its localization to the nucleus. For legume TFs, this has been done with immunohistochemical localization (Rodriguez-Uribe and O'Connell, 2006) or using GFP or GUS fusion proteins (Kim et al., 2001; Kaló et al., 2005; Smit et al., 2005; Wang et al., 2005; Shukla et al., 2006). In the case of NSP2, a regulator of legume-rhizobium symbiosis, nuclear relocalization was detected following application of purified Nod factors, suggesting that posttranslational modification is required to activate this protein (Kaló et al., 2005).

So far, there has been a major disconnect between TFs that have been ascribed a biological role based on genetic data and TFs that have been characterized at the biochemical and/or molecular levels. Clearly, to understand better the function of genetically characterized TFs, we need to identify the genes and network of genes that they control. On the other hand, for TFs that have been characterized in terms of their DNA-binding ability, it is now important that biological function be established via forward or reverse genetics. Furthermore, despite the knowledge that TFs often work as part of a team or complex of proteins to recruit or block recruitment of RNA polymerase to the DNA (Lee and Young, 2000), virtually nothing is known about the proteins that interact with legume TFs to ensure their biological activity. Tissue and organ development and differentiation and plant responses to specific environmental challenges require the concerted activity of networks of TFs, which orchestrate global changes in transcription. The details of these networks remain unknown in legumes. Addressing these open questions in legume TF biology in an efficient manner will require a coordinated effort on the part of the scientific community. The final section of this review offers a roadmap for this enterprise.

	A ROADMAP FOR FUTURE RESEARCH ON LEGUME TFs

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Within the next 2 or 3 years, complete or near-complete genomic sequence for the euchromatic regions of three legumes, Medicago, Lotus, and soybean, will be available. This will greatly facilitate systematic approaches to TF functional analysis. Bioinformatics approaches will rapidly identify putative TFs among the new genomic sequences, as described above, which will provide grist for the functional analysis mill. Whereas forward genetics will gather momentum as genomic sequencing results in more complete and better integrated physical and genetic maps of chromosomes, which will facilitate map-based cloning of additional TFs involved in legume development and differentiation, reverse-genetics approaches are likely to play a more significant role in the functional characterization of TFs in the future. Certainly, reverse genetics offers a more systematic way to characterize all putative TF genes.

Some of the tools for systematic reverse-genetics analysis of TF function in legumes, such as plant transformation protocols for RNAi and overexpression (Thykjaer et al., 1997; Chabaud et al., 2003; Ott et al., 2005; Zhang et al., 2005) and ethyl methanesulfonate mutant populations for TILLING (Perry et al., 2003), are already in place. Others, such as transposon-insertion (Tadege et al., 2005) and fast neutron bombardment deletion mutant populations (Wang et al., 2006) are being developed, and a mutant from a small Tnt1 insertion population has already been described (Benlloch et al., 2006). Viral-induced gene silencing is another promising tool for high-throughput reverse genetics that has proven successful in pea (Constantin et al., 2004).

In view of the TF content of Arabidopsis and rice, we expect that each of the three model legumes mentioned above will possess at least 2,000 TF genes. It will be an impossible task for any one group to characterize this number of genes, at least at the genetic level. A coordinated international effort would help to make the process of TF gene function discovery most efficient. One way to give direction to such an enterprise would be to determine first the developmental and environmental expression profiles of each TF in the context of the whole transcriptome. This would serve several purposes. First, it would reveal any organ/developmental specificity. Second, it would reveal any environmental stress specificity, which would constrain hypotheses about possible roles of each TF. Third, by setting TF gene expression profiles into the broader, whole-genome context of transcription, correlations between individual TFs and groups of other genes would be revealed, which would help to refine hypotheses about possible TF function, especially if correlated sets of genes are predicted to be involved in one or just a few biological processes. Many of the tools required for such transcriptome analyses are now available for Medicago, Lotus, and soybean, including Affymetrix GeneChips containing probe sets for the majority of genes in these three models. In addition, we are currently developing gene-specific primers for all Medicago TFs for qRT-PCR to complement data obtained using the corresponding Affymetrix GeneChip (K. Kakar and M.K. Udvardi, unpublished data), and a similar resource is being developed for soybean (G. Stacey, personal communication). Transcript quantification by qRT-PCR is more sensitive than by DNA array hybridization methods (Czechowski et al., 2004) so the resources being developed for qRT-PCR profiling in Medicago and soybean will provide a more comprehensive picture of TF expression patterns in this species. Hierarchical cluster analysis (Yu et al., 2005) and Pearson correlation (Zar, 1999; Persson et al., 2005) are two ways to identify genes that are coordinately regulated, which will not only provide clues about the possible function of TF genes (see above), but also identify possible downstream target genes of specific TFs.

There have been few attempts to confirm the physical interaction between a genetically characterized legume TF and a target gene, although possible target genes have been identified by transcriptome analysis of TF mutants (e.g. Kaló et al., 2005; Smit et al., 2005). Methods have been developed to identify TF target genes in a nonbiased, high-throughput manner. Perhaps the most powerful of these is chromatin immunoprecipitation (ChIP) followed by DNA array hybridization (called ChIP-chip) to identify DNA fragments covalently bound to immunoprecipitated DNA-binding proteins (Thibaud-Nissen et al., 2006). Specific immunoprecipitation can be facilitated by in planta expression of the TF of interest as a fusion protein with a short, nonplant peptide epitope at one end, which enables the use of commercially available monoclonal antibodies directed toward the epitope to precipitate the fusion protein and any covalently linked proteins and DNA. This approach has been used, for example, to identify genomic DNA bound by the Arabidopsis FLC TF (Helliwell et al., 2006). Affinity purification can also be used to identify associated proteins in DNA-binding complexes (Wood et al., 2006). A prerequisite for ChIP-chip is an array containing probes for promoter DNA. Arrays designed to detect gene transcripts, such as the Affymetrix GeneChips for Medicago, Lotus, and soybean, are not suitable for such applications. However, tiling arrays, which contain oligonucleotide probes covering the entire genome (coding and noncoding) with short or no gaps between probed sequences are well suited to ChIP-chip (Thibaud-Nissen et al., 2006; Zhang et al., 2006). Although no tiling array exists for a legume yet, we have plans to develop a Medicago tiling array upon completion of the genome sequence in 2008.

The preceding paragraphs may give the impression that the road is mostly clear for rapid progress in TF function discovery in model legumes. However, it is likely that there will be bumps, potholes, and unexpected turns in the road ahead. For instance, some TFs appear to job share with one or more close relatives, so that loss of function of one gene may go unnoticed in a mutant plant (Riechmann and Ratcliffe, 2000). Functional redundancy between some TFs makes it difficult, if not impossible, to isolate mutations in these genes via forward genetics. However, reverse-genetics approaches that utilize phylogenetic and transcriptomic information to identify potentially redundant genes prior to the creation of double or higher order mutants should overcome this problem (e.g. Liljegren et al., 2000; Zhang et al., 2003). Obviously, the availability of well-curated mutant populations (see above) will be essential for this endeavor. An alternative approach to overcome functional redundancy is to create dominant-negative mutants by fusing TFs to known repressor domains (Markel et al., 2002). Yet another approach is to overexpress the TF of interest in transgenic plants and to monitor the effects of this on the expression of other genes and on the phenotype (biochemical, physiological, developmental, or otherwise) of the altered plants. Ideally, TF overexpression should be confined to the same cell, tissue, and organ types as the endogenous gene and preferably under the control of an inducible promoter. There is mounting evidence that diversification of TF function in plants often results from changes in nontranscribed sequences that alter the expression domain of the gene, rather than from changes in the coding sequence that alter the DNA- or protein-binding properties of TFs. Thus, TF mutant phenotypes have been suppressed by ectopic expression of related TFs that are not normally expressed in the same tissue/organ as the mutated TF (Riechmann, 2002). Overexpression of TFs can also interfere with processes totally unrelated to the normal function of the protein (Riechmann and Ratcliffe, 2000). Clearly, care must be taken in designing and interpreting TF overexpression experiments.

TFs interact physically with other proteins, in addition to the RNA polymerase complex itself, to effect changes in gene transcription (Lee and Young, 2000). The specific makeup of these complexes is unknown for the majority of plant genes, although this knowledge is a prerequisite to understanding the combinatorial control of transcription (Singh, 1998). Approaches such as yeast two-hybrid screening (e.g. Zhang et al., 1999) and ChIP followed by proteomic analysis of the resulting protein complexes (Helliwell et al., 2006; Wood et al., 2006) will be useful in this context. Finally, the network of genes regulated by a single TF and its partners is just a small part of a larger genetic regulatory network that ensures coordinated expression of genes involved in many different cellular processes during plant development and differentiation. Deciphering these global genetic networks will require integration of many of the genomic, functional genomic, and bioinformatic approaches described above.

Supplemental Data

The following materials are available in the online version of this article.

Supplemental Table S1. Putative TFs among IMGAG-annotated proteins.

Received February 14, 2007; accepted March 24, 2007; published June 6, 2007.

	FOOTNOTES

 
¹ This work was supported by the Samuel Roberts Noble Foundation, the Max Planck Society, the European Union FP6 Program, and U.S. Department of Agriculture Cooperative State Research, Education, and Extension Service-National Research Initiative.

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Michael K. Udvardi (mudvardi{at}noble.org).

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

www.plantphysiol.org/cgi/doi/10.1104/pp.107.098061

^* Corresponding author; e-mail mudvardi{at}noble.org; fax 580–224–6692.

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TOP THE DYNAMIC TRANSCRIPTOME IDENTIFICATION OF PUTATIVE TFs FUNCTIONAL CHARACTERIZATION OF... A ROADMAP FOR FUTURE... LITERATURE CITED

 
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