Legume Transcription Factor Genes: What Makes Legumes So Special?
Year: 2009
Type: article
Abstract: All eukaryotic organisms have a diversity of transcription factor (TF) gene families, encoding key proteins regulating gene expression. TF families are strongly conserved across eukaryotic organisms, especially plants. The specific function of each of these TF genes is of interest due to their role in controlling plant developmental processes and responses to environmental conditions, including functions of key importance to agronomic performance. In this review, we focus on the role of TF genes in legume species. The review also provides an update on the identification and categorization of TF genes in several eukaryotes, including three partially or completely sequenced legume genomes (soybean [Glycine max], Medicago truncatula, and Lotus japonicus). The role of TF genes in legumes is discussed in an evolutionary context based upon a comprehensive comparison of TF gene distribution and direct experimental data obtained for a significant number of legume TF genes. TF genes are present in all eukaryotic phyla. They encode regulatory proteins that interact with genomic DNA promoter and enhancer sequences. These interactions facilitate the transcriptional activation or repression of proximal genes and enable cells to respond to changes in their environment (e.g. biotic and abiotic stresses), to regulate the cell cycle, and, in the case of the most complex organisms, to control cell fate. As mentioned by Carroll (2001), the expansion of regulatory protein numbers and interactions, as well as changes to their spatial and temporal expression, is part of the evolutionary process leading to increasingly complex organisms. Therefore, determining the repertoire of TF genes in genomes, the regulation of their expression, and their biochemical properties (i.e. DNA- and protein-binding affinities) is important to the understanding of TF regulatory networks and organism evolution. The immobile nature of plants represents a major disadvantage compared with animals, which can flee many environmental assaults. The ability to face environmental challenges implies that plants must possess complex regulatory systems to respond appropriately. This sometimes involves changing developmental programs, which is facilitated by the fact that plants maintain active stem cells, called meristems, which can differentiate and develop into various organs depending on environmental and endogenous cues. As regulators of transcription, TFs play important roles in helping plants meet and master environmental challenges. Therefore, it is not surprising that plants have more TF genes than animals (Riechmann et al., 2000; this study). Most of the extant knowledge of plant TF genes was obtained from studies of the major genetic model in plant biology, Arabidopsis (Arabidopsis thaliana). However, while Arabidopsis is a useful model for many developmental and other processes common to all higher plants, it lacks certain traits that are of immense value to agriculture, such as the ability to form nitrogen-fixing symbioses with rhizobia and soil nutrient-scavenging symbioses with mycorrhizal fungi. Legumes, on the other hand, are able to establish such beneficial symbioses and, as a result, have been mainstays for sustainable agriculture for thousands of years. The legume family includes important food plants such as common bean (Phaseolus vulgaris), soybean, and pea (Pisum sativum) and important forage species such as alfalfa (Medicago sativa) and clover (Trifolium spp.). There is also growing interest in the use of legumes as a source of biomass for biofuel production. Although mycorrhizal symbioses are widespread among plant families, occurring in approximately 90% of all species, symbiotic nitrogen fixation (SNF) is restricted to legumes and a few nonlegume families. This makes legumes special, but just how SNF evolved in legumes remains largely unknown. Answers to this question may emerge from comparative analysis of the genomes of legumes and nonlegumes. Genome sequencing of three legume species, L. japonicus (http://www.kazusa.or.jp/lotus), soybean (http://www.phytozome.net/soybean), and M. truncatula (http://www.medicago.org/genome), is nearing completion, and the genome sequences of several nonlegumes, including Arabidopsis (Arabidopsis Genome Initiative, 2000), Vitis vinifera (Jaillon et al., 2007), Sorghum bicolor (Paterson et al., 2009), Physcomitrella patens (Rensing et al., 2008), Chlamydomonas reinhardtii (Merchant et al., 2007), Oryza sativa (Yu et al., 2002), and Populus trichocarpa (Tuskan et al., 2006), are known (Table I Classification of main plant species based on their class, order, family, and genus The genome size, ploidy level of each genome, number of predicted protein-coding genes, and number of TF genes identified are also indicated. Classification of main plant species based on their class, order, family, and genus The genome size, ploidy level of each genome, number of predicted protein-coding genes, and number of TF genes identified are also indicated. Given the central role of TFs in regulating plant gene expression and consequently development, differentiation, and responses to the environment, as well as their key roles in evolution (Ramalingam et al., 2003; Miller et al., 2006; Francia et al., 2007), the set of genes encoding TFs is an obvious place to start looking for evolutionary innovations that define key legume traits, such as SNF. More generally, the study of legume TFs will shed light on their roles in plant processes common to all plant species. When comparing legumes with other plant phyla, a key question is, “What traits define a legume” This question was raised several years ago by Doyle and Luckow (2003) and by Zhu et al. (2005). Morphogenesis and life styles of different plant species and more generally of eukaryotes depend heavily on the control of gene expression. Therefore, it can be assumed that the repertoire of TF genes within a plant species, their expression pattern, and their function largely determine the unique aspects of the species. Unfortunately, as discussed below, the functions of only a few legume TF genes are known. Therefore, a tremendous effort is required to characterize the role of TF genes in legumes. The emerging high-throughput genome-based technologies that build upon the sequencing of several legume genomes open new fields of investigation, including a complete identification and classification of legume TF genes. In this review, we summarize knowledge of legume TFs while updating the classification of legume, nonlegume, and nonplant eukaryotic TF genes. Legume TF function and TF gene expression are also discussed in the light of recently published studies. Altogether, these data will be discussed in an evolutionary context to better understand the impact of TF genes on legume development. The last comprehensive review of legume TFs predated the completion of any of the legume genome sequencing projects but noted that more than 99% of predicted legume TFs remained to be characterized functionally (Udvardi et al., 2007). In the interim, the genome sequences of three legumes have been completed, or nearly so, enabling both comparative and functional genomics studies, and the roles of new legume TFs have been determined. Recent studies have elucidated the roles of several TFs in legume development. Initially, several legume TF genes were identified based upon similarity of mutant phenotypes in legumes and Arabidopsis and sequence homology between legume genes and the Arabidopsis genes known to confer specific mutant phenotypes. Legume TF genes discovered in this way include those involved in the control of floral meristems, such as LjFLO, PsFLO/LFY, PsPEAM4, and MtPIM (Hofer et al., 1997; Berbel et al., 2001; Taylor et al., 2002; Dong et al., 2005; Benlloch et al., 2006). In the same way, three L. japonicus MYB TFs with homology to Arabidopsis TRANSPARENT TESTA2 (AtTT2) were shown to regulate proanthocyanidin biosynthesis after their transient expression in Arabidopsis leaves (Yoshida et al., 2008). More recently, the role of legume TF genes was investigated using reverse-genetic approaches. For example, expression of the soybean GmWRKY13 gene in Arabidopsis positively affected lateral root formation (Zhou et al., 2008). RNA interference knockdown of MtSERF1, which encodes an AP2-EREBP TF, altered the production of somatic embryos (Mantiri et al., 2008). Legume TF genes were also recently implicated in responses to environmental challenges. For instance, after identifying TF genes regulated in response to phosphate deprivation in common bean (Hernández et al., 2007), Valdés-López et al. (2008) characterized the role of one MYB TF, PvPHR1, as a key protein in phosphorus uptake. Similarly, after quantifying the expression levels of soybean Dof genes in various organs, including flowers and pods, the overexpression of GmDof4 and GmDof11 TF genes in Arabidopsis was shown to increase seed lipid content (Wang et al., 2007). A large number of studies also highlighted the role of legume TF genes in plant responses to abiotic stresses. For example, a common method for examining gene function is to overexpress the gene of interest from a strong, constitutive promoter (e.g. cauliflower mosaic virus 35S) and then to gauge the response of the resulting transgenic plants to a variety of treatments (e.g. abiotic stress). For example, the overexpression of two TFIIIA-related TF genes (MtZPT2-1 and MtZPT2-2) in M. truncatula led to an increase in the size of the plant root system under salt stress (de Lorenzo et al., 2007). GmWRKY54 and GmDREB2 increased tolerance to both salt and drought when overexpressed in Arabidopsis (Chen et al., 2007; Zhou et al., 2008). In the same study, Zhou et al. (2008) also implicated two other WRKY TF genes, GmWRKY21 and GmWRKY13, in tolerance to cold, salt, and mannitol stresses by overexpressing these genes in Arabidopsis plants. A similar approach established a role for GmDREB3 in Arabidopsis tolerance to cold, drought, and high-salt stresses (Chen et al., 2009). Zhu et al. (2006) observed a higher tolerance of soybean plants to high temperature following overexpression of the GmHSFA1 TF gene. Interestingly, Zhang et al. (2008) identified two GmAP2-EREBP TF genes involved not only in abiotic stress response but also in plant-pathogen defense mechanisms. Overexpression of GmAP2-EREBPs in tobacco (Nicotiana tabacum) enhanced plant resistance to drought, salt stress, and pathogen infection. This study suggested that some TF genes are central to the general plant stress response. With regard to pathogen response, Park et al. (2007) reported that GmZF-HD1 and GmZF-HD2 were induced in response to Pseudomonas syringae infection. In addition to the activation of plant defense systems through the activation of TF genes, legume TFs are also involved in the control of mutualistic interactions between plant root and soil microorganisms. For example, nodulation involves the interaction between root and soil bacteria leading to SNF. This complex interaction is mainly restricted to legumes and, for this reason, makes legumes special. The infection of plant roots by symbiotic bacteria begins by the invasion of root hair cells by the symbiont through the newly formed infection thread. This infection is dependent on several genes. Genes that are specifically expressed during nodulation are termed nodulins. Several years ago, protein factors that bound to the AT-rich promoter sequences of nodulin genes were identified (Jensen et al., 1988; Metz et al., 1988; Forde et al., 1990; Laursen et al., 1994; Hansen et al., 1999). More recently, TF genes specifically involved in the rhizobial infection process have been identified. Among them, the M. truncatula NSP1 and NSP2 genes, which encode two GRAS TFs, are essential to root hair infection. The root hairs of Mtnsp1 and Mtnsp2 mutants are not infected by the symbiont (Catoira et al., 2000; Oldroyd and Long, 2003). More recently, based on a mutant screen for plants lacking infection threads upon inoculation with rhizobia, the L. japonicus NSP1 and NSP2 genes were identified (Heckmann et al., 2006). The first TF shown to have an essential role in nodulation was the L. japonicus NIN gene (Schauser et al., 1999). Mutations in this gene abolish both infection and the induction of nodule primordia. However, NIN appears to act downstream of the initial steps in symbiont recognition by the plant (Oldroyd and Downie, 2008). By screening fast-neutron and Tnt1 transposon-tagged mutagenized populations, Marsh et al. (2007) characterized the M. truncatula ortholog of LjNIN (Catoira et al., 2001). The PsSym35 locus defines the pea NIN ortholog (Borisov et al., 2003). The likely soybean ortholog of NIN is clearly evident in the soybean genomic sequence, and this genomic region shows significant microsynteny to the NIN-encoding regions of M. truncatula and L. japonicus (M. Libault, X.C. Zhang, and G. Stacey, unpublished data). Additional TF genes critical to the nodulation process were also identified by direct screening for nodulation-defective mutants. For example, this approach led to the identification of the L. japonicus ASTRAY gene encoding a bZIP TF (Nishimura et al., 2002). L. japonicus mutants a (i.e. increased nodule Similarly, et al. (2007) identified the encoding an AP2-EREBP TF, as for invasion of plant cells by symbiotic an AP2-EREBP TF gene was identified as a of nodulation in L. japonicus et al., 2008). also the identification of important TF genes involved in For example, based on interaction with critical for rhizobial et al., 2002), Zhu et al. (2008) identified a protein for role during nodulation that encodes an The that the expression of the NIN gene. et al. DNA analysis to several genes regulated during M. truncatula including an AP2-EREBP TF gene on the of an as well as plants for expression or overexpressing the et al. (2008) as an important controlling infection of M. In the roles of a of TF genes in a variety of legume Overexpression of legume TF genes in nonlegume plants phenotypes with of TF function among higher plant species. the of TF gene families across the plant it is that legumes while most other plant species Although specific TF genes have been implicated in nodule development, these to families common to nonlegumes. This that of TF genes was important in the evolution of than the of TF better understand the evolution of TFs, comparative studies of TF gene families of several organisms, including have been (Riechmann et al., However, genome sequences from plant species and of TFs in and have such studies genome sequences of a large diversity of organisms, including several plant species, have been or will be (Table The of genomic sequences with the use of gene (e.g. and protein function (e.g. et al., et al., and a more complete identification of the gene content in each genome, including TF genes. are well by the of gene sequencing on such it is to characterize the TF gene of a few plant species, as as known TF families are and in TF gene among eukaryotes, and more specifically among plants, may to the “What makes a legume a legume” and 2003). of TF genes in of the main eukaryotic organisms TF proteins were identified for model Chlamydomonas reinhardtii Physcomitrella patens Oryza sativa Sorghum bicolor Arabidopsis Populus trichocarpa Medicago truncatula Lotus japonicus and Vitis vinifera The TF genes were across families based on the identification of the TF family protein et al. and the et al., were as for this The is based on and in and light and in and of TF genes in of the main eukaryotic organisms TF proteins were identified for model Chlamydomonas reinhardtii Physcomitrella patens Oryza sativa Sorghum bicolor Arabidopsis Populus trichocarpa Medicago truncatula Lotus japonicus and Vitis vinifera The TF genes were across families based on the identification of the TF family protein et al. and the et al., were as for this The is based on and in and light and in and of TF gene distribution based on family across different eukaryotic species. For each species, the of each TF family in the of TF genes identified was expressed as a The the of The was using the between each organism using the the distribution of genes among the TF families families are specific to plants and families are specific to animals (Table families are in while one TF family is in families were common to all in this TF gene family was which may the of knowledge legume TFs but more likely of TF families among plants. with this the distribution of legume genes among the various TF families is similar to that of other plant species. based on this of genes in the various TF families, not to be any of known TF families in legumes. The of significant in TF gene distribution across TF families between legume and nonlegume plants that traits are likely dependent on TF gene expression and TF protein most of the plant TFs characterized to Therefore, an is to the knowledge established in Arabidopsis to legume TFs (Hofer et al., 1997; Berbel et al., 2001; Taylor et al., 2002; Dong et al., 2005; Benlloch et al., 2006). The expression of legume TF genes in Arabidopsis or tobacco plants also a of functions for TF across plant species (e.g. in plant Zhou et al., biosynthesis TFs to et al., plant resistance to Zhang et al. and plant resistance to abiotic stresses Zhou et al. et al., However, complete functional of TF proteins between plants is not For example, the gene encoding a MYB TF gene in Arabidopsis but it not this when expressed in M. truncatula et al., 2009). upon these few TF function appears but not conserved across plant species. This is also by the of TF protein and the of TFs However, one in this is the identification of between plant species. As below, due to the evolutionary between plants, are to For example, in the Arabidopsis and legumes in the and the (Table These two approximately to years ago to et al. a of than after the between and the in and development. This evolutionary between plants and Arabidopsis is also highlighted by the changes in the size and of their genomes (Table such as the genome in legumes occurring to et al., 2005; et al., by a more in soybean to et al., 2007). the evolutionary between legumes and microsynteny is in some regions et al., 2000; et al., 2003). For example, of microsynteny between Arabidopsis and soybean et al., 2003; et al., et al., a comparison between soybean, and Arabidopsis identified two with microsynteny et al., 2007). between Arabidopsis and legumes is to due to genome and gene et al., 2005; et al., 2008). between legume species et al., et al., 2006; for review, and 2009). The of between legumes will be an important for to soybean, an important from the knowledge established in the legume M. truncatula and L. The fact that all major legume genetic M. truncatula, soybean, and common in the one of the three of legumes (i.e. legumes are into three and the in the legume genome sequences. The from the two other legume approximately while the Lotus and Medicago from one 2003). This among major legumes makes it to by direct genome For example, this approach the identification of key TF gene involved in the nodulation process and in floral (e.g. LjNIN and and and and and et al., 1997; et al., et al., 2000; et al., 2003; Oldroyd and Long, 2003; Dong et al., 2005; et al., 2005; et al., 2005; et al., As legume TF distribution across families and their functions to be conserved compared with other plant families. legume traits may from unique TF gene expression the last the of and the of gene expression in a large number of organisms in different and under environmental However, several studies clearly the of this to the expression of such as TF genes et al., et al., 2007). better characterize the expression of TF genes, were to TF gene expression in M. truncatula, soybean, and L. japonicus et al., et al., 2007; et al., et al., and unpublished data). Several studies these to TF gene expression in different and in response to different treatments et al., 2005; et al., 2007; et al., et al., 2009). to the use of sequencing such as the et al., and et al., an of These the of the TF gene However, the use of such is only the genome of the organism of interest is sequenced and the of gene expression as a for we investigated the expression of of the gene This family was based upon the of some of in root hair infection and nodule (Schauser et al., et al., 2001; et al., Marsh et al., 2007). studies place NIN gene function just downstream to NSP1 and NSP2 GRAS in the regulating legume For example, LjNIN gene expression is under the control of et al., 2006). and interact with the gene promoter to regulate expression et al., 2009). In the same study, et al. that the interaction of and was also required to gene expression during In et al. (2006) that gene expression was under the control of a to legume nodulation et al., 2007; et al., 2008). soybean, L. and M. truncatula gene expression in various plant expression levels of Arabidopsis soybean L. japonicus and M. truncatula genes are reported for different root and For each plant species, the of the genes is reported on the are in Genes encoding proteins a are highlighted by LjNIN (Schauser et al., and et al., involved in nodulation are was also strongly expressed in soybean and root is not a analysis of TF genes among the sequenced plant genomes not a family, it a specific TF family that appears to have been in legumes. However, legumes have clearly in specific traits by some TF genes for a more In the case of TFs, this likely involved changes in the sequences of that activation of gene expression during nodule development. is is a of the legume TF gene and of the by each The legume TF be elucidated with the of sequencing the of a TF the important an will interactions as well as interactions will the of legume gene on bacteria and cells have established interaction the first into the of these systems et al., et al., et al., 2009). The in identification of regions of TF genes is by with the use of after sequencing of the genome et al., 2008). The most approach with sequencing technologies and 2009). These the identification of promoter that interact with TF proteins with to In are an important for regulation of gene expression the level by controlling to and 2006). TF and data in the context of will a of legume gene are a family of plants in to their ability to develop unique organs, called which nitrogen-fixing Among the genes involved in the nodulation several TFs have been The similar distribution of TF genes in the various known TF families in legumes and nonlegumes, as well as the conserved nature of their biochemical how traits such as SNF upon analysis of the TF family in soybean, L. M. truncatula, and we that legumes TF genes for use in processes by their expression of between legume and nonlegume plants and of the expression of TF genes will to this identification of sequences of TF proteins and analysis of TF gene expression will a to understand the impact of TF on the legume The following are in the of this levels of soybean, L. and M. truncatula genes to
Source: PLANT PHYSIOLOGY
Institutions: Noble Research Institute, University of Missouri
Language: English
Subfield: Plant Science
Domain: Life Sciences
SDG: Zero hunger
Open Access status: green
OpenAlex ID: W2106294566