Genome-wide evolutionary characterization and analysis of bZIP transcription factors and their expression profiles in response to multiple abiotic stresses in Brachypodium distachyon
© Liu and Chu; licensee BioMed Central. 2015
Received: 15 August 2014
Accepted: 9 March 2015
Published: 22 March 2015
Plant basic leucine zipper (bZIP) transcription factors are one of the largest and most diverse gene families and play key roles in regulating diverse stress processes. Brachypodium distachyon is emerging as a widely recognized model plant for the temperate grass family and the herbaceous energy crops, however there is no comprehensive analysis of bZIPs in B. distachyon, especially those involved in stress tolerances.
In this study, 96 bZIP genes (BdbZIPs) were identified distributing unevenly on each chromosome of B. distachyon, and most of them were scattered in the low CpG content regions. Gene duplications were widespread throughout B. distachyon genome. Evolutionary comparisons suggested B. distachyon and rice’s bZIPs had the similar evolutionary patterns. The exon splicing in BdbZIP motifs were more complex and diverse than those in other plant species. We further revealed the potential close relationships between BdbZIP gene expressions and items including gene structure, exon splicing pattern and dimerization features. In addition, multiple stresses expression profile demonstrated that BdbZIPs exhibited significant expression patterns responding to 14 stresses, and those responding to heavy metal treatments showed opposite expression pattern comparing to the treatments of environmental factors and phytohormones. We also screened certain up- and down-regulated BdbZIP genes with fold changes ≥2, which were more sensitive to abiotic stress conditions.
BdbZIP genes behaved diverse functional characters and showed discrepant and some regular expression patterns in response to abiotic stresses. Comprehensive analysis indicated these BdbZIPs’ expressions were associated not only with gene structure, exon splicing pattern and dimerization feature, but also with abiotic stress treatments. It is possible that our findings are crucial for revealing the potentialities of utilizing these candidate BdbZIPs to improve productivity of grass plants and cereal crops.
In plants, the leucine zipper (bZIP) transcription factors are one of the largest and most conserved gene families and play key roles in regulating diverse biological processes [1-5]. The bZIP domain contains about 60 to 80 amino acids and characteristically harbors two distinct function regions: a highly conserved basic region N-x7-R/K-x9 and a less conserved leucine zipper coiled-coil motif . And the basic region and leucine zipper coiled-coil motif region was linked by a hinge region. The bZIP proteins bind to DNA by forming heterotypic or homotypic complexes [7,8]. The basic region is responsible for nuclear localization and DNA binding specifically, and the following leucine zipper motif consisting of several repeats of leucine or other hydrophobic amino acids and grant for recognition and dimerization specificity . The intron patterns within the basic and the hinge region are very important for their functional evolution due to different status of exon splicing in these regions. In plant species such as rice, maize and Arabidopsis, the patterns of those motifs exhibited regular conservation and diversity [10,11]. The bZIP proteins are dimerized transcription factors in all eukaryotes, and the leucine zipper is responsible for the dimerization of bZIP proteins. The rules of dimerization specificity for bZIP proteins have been depicted [12-14]. Depend upon the basis of the presence of attractive or repulsive interhelical g↔e electrostatic interactions and the presence of polar or charged amino acids in the a and d positions of the hydrophobic interface of the leucine zipper region, dimerization specificity of bZIP proteins in plant species such as Arabidopsis, maize and rice have been predicted [10,11,15].
The evolution of genetic network complexities in flowering plants has revealed the important roles of regulatory transcription factor evolution to physiological variation among species [16,17]. As one of important transcription factor family, the plant bZIP transcription factors play pivotal roles in developmental processes and multiple stresses in response to environmental tolerance. The ancestor of green plants possessed four bZIP genes functionally involved in oxdative stress and unfolded protein responses that are bZIP-mediated processes in all eukaryotes . Furthermore, bZIP genes regulate diverse biological processes such as seed development, flower maturation, pathogen defense, and light and stress signaling [3,6]. Fundamentally, various transcription factors had been observed to regulate the ABA-responsive gene expression [19,20]. The transcriptional drought, cold, and salinity stress gene expression have been concluded . So far, members of bZIP transcription factors have been identified or predicted in most of plant species analyzed [22-26]. In cucumber, 64 bZIPs were observed and all of the select genes displayed down-regulated with PEG treatment . In maize, ZmbZIP17 functions as an endoplasmic reticulum stress transducer and interact with ABA-responsive cis-elements (ABRE) . In rice, plenty of OsbZIPs displayed different expression patterns when dealed with cold or salt stresses . OsbZIP71 was strongly induced in ABA-mediated drought and salt tolerance in rice . OsbZIP46 expression was strongly induced by drought, heat, and ABA, and functions as a positive regulator of ABA signaling and drought stress tolerance of rice depending on its activation . OsbZIP52/RISBZ5 could function as a negative regulator in cold and drought stress environments . A bZIP gene ABI5 played an important role in ABA-arrested seed germination, was robustly associated with the flower transition in Arabidopsis . A bZIP gene ThbZIP1 from Tamarix hispida in response to abiotic stresses had been characterized and showed to have an increased tolerance to drought and salt. Microarray analysis had been shown that many ROS scavenging genes were up-regulated by ThbZIP1 under salt stress conditions . MabZIP3 was isolated from banana fruit, it was responsive to MeJA, ABA, and chilling stress . As the most dangerous pollutions, heavy metals had been regarded as the new stress factors affecting the growth of plants. Foods contaminated with heavy metal tolerance profile of different native or gene-modified plant species had been applied [33-39]. Though studies had shown that bZIP transcription factors played key roles when plants grew under environmental factors and phytohormones, there was few research of bZIP genes study in heavy metal stresses so far.
B. distachyon is a new emerging model plant of Poaceae family and the first species of sequenced grass subfamily Pooideae . Due to its high efficiency for genetic manipulation and compact genome, B. distachyon has become more crucial in applied functional genomics . Researches on B. distachyon are moving forward rapidly, and the research field has covered grain development and starch deposition, biotic and abiotic stress responses, and biofuel production [42-44]. Global gene expression in B. distachyon had revealed extensive network plasticity in response to abiotic stress . Evolutionary studies on bZIP gene families had been shown that a shifting landscape of biochemical functions related to signaling and gene expression contributed to species diversity . Although these studies reported were involved in various plant species, none of researches were associated with the evolution and the molecular biology of stress in detail, especially in the grain model plant B. distachyon. There is no investigation of bZIP transcription factors in B. distachyon so far. Understanding the detailed evolutionary history of BdbZIPs and their corresponding functions in stress biology is of great importance in B. distachyon.
In this study, we identified BdbZIP genes genome-widely in B.distachyon and further investigated their chromosomal localization and evolutionary relationship with their counterparts from monocot O. sativa and dicot A. thalinana. We analyzed their exons splicing of basic and hinge region of bZIP domain, which are very important for bZIP functional evolution. We also characterized dimerization pattern within the leucine zipper motif and gene structures, and obtained tissue-specific gene expression profile and genes expression profile responding to multiple stresses including environmental factors, phytohormones, and heavy metals. This study increased our understanding of BdbZIP family genes associated with stress adaptation and tolerance, which was crucial for further study to improve the productivity of grass plants and cereal crops.
Plant growth condition and treatments
The seeds of B. distachyon Bd21-3 were surface sterilized with 20% NaOCl and planted on 0.6% agar containing 0.5× Murashige and Skoog and 0.3% Sucrose. Plants were grown at 22°C under 16-h-light/8-h-dark conditions and the light intensity was 120 μm m−2 s−1. As for stress expression analysis, 2-week-old seedlings were treated with 3 major treatment groups including group 1-environmental factors ( cold, heat, H2O2, PEG, and NaCl), group 2-heavy metals (Cu, Zn, Mn, Cd, and Pb) and group 3-phytohormones (SA, 6-BA, ABA, and MeJA) (As for detailed treatments, please refer to Additional file 1: Table S1).
bZIP sequence extraction and structure analysis
The sequences of B. distachyon bZIP genes were obtained from BGD (Brachypodium Genome Database) (http://Brachypodium.org) and Plant Transcription Factor Database verition 3.0 (Plant-TFDB 3.0) (http://planttfdb.cbi.pku.edu.cn) . The Arabidopsis and rice bZIP genes were retrieved from The Arabidopsis Information Resource (TAIR), Plant-TFDB and National Rice Gene Database (http://www.ricedata.cn/gene). The status of intron and exon were annotated according to the database. All bZIP domains were verified by SMART (http://smart.embl-heidelberg.de) and Pfam (http://pfam.sanger.ac.uk). All BdbZIP motifs were analyzed by MEME (http://meme.nbcr.net/meme). The limits of minimum width, maximum width and maximum number of motifs were specified as 10, 50 and 50 respectively. Fifteen motifs including bZIP domain were finally verified with the low E-value (<−43). The motifs were numbered according to their order displayed in MEME.
Phylogenetic and molecular evolutionary analyses were calculated in MEGA 5.0 package by using the p-distance model, and the Neighbor-joining statistical method followed by 1000 bootstrap replications were applied . The bZIP protein sequences of B. distachyon, Arabidopsis and rice were loaded into MEGA 5.0. In addition, homology searches were performed in rice and Arabidopsis with BLAST, and the SCORE value and E-value were taken into account for judging the homologous genes. bZIP gene duplication events among B. distachyon, Arabidopsis and rice were analyzed through Plant Genome Duplication Database (http://chibba.agtec.uga.edu/duplication) . The Ka and Ks values were listed as Additional file 1: Table S2. The data of the phylogenetic tree was deposited in Treebase Web (Accession URL: http://purl.org/phylo/treebase/phylows/study/TB2:S17110).
Chromosomal distribution and duplication of BdbZIPs
The location information of each BdbZIP gene on each chromosome was detected from BGD (Brachypodium Genome Database). The genetic linkage map was constructed with MapDraw . The number of CpG in every 100 kb scale was measured and the status of CpG content was constructed by PermutMatrix. Every duplicated BdbZIP gene pairs were put in same bracket.
Expression data analyses
To analyze tissue (root, stem, leaf and early spikelet) specific expression, 2-week-old seedlings and early spikelets from 5-week-old of B. distachyon were sampled. Total RNA was extracted as described previously . The cDNA was synthesized with 3.0 μg of total RNA by using PrimeScript Reverse Transcriptase (TAKARA). The reaction mixtures were diluted 20 times with distilled water and used as templates for quantitative real-time PCR. The primers used in this paper were listed in Additional file 1: Table S3. The qPCR was conducted and repeated three times. The reaction condition was as follows: 95°C for 3 mins, 40 cycles of 95°C for 10 s, 55°C for 30 s. The expression profiles were calculated with –ΔΔCT values. Fold changes were also calculated with the formula “fold change = 2–ΔΔCT”. Expression data and hierarchical clustering analysis of all the samples were carried out using PermutMatrix 1.9.3, and shown with green-red gradient. The up-regulated genes were defined as a fold change of ≥ 2 with p-value <0.05 and marked with red color, and a fold change of ≤ 0.5 were defined as down-regulated genes with p-value <0.05 and marked with green color. All qPCR data were submitted to NCBI GEO dataset. The accession number is GSE66458.
Results and discussion
Identification of bZIP genes in plants
Chromosomal location and duplication of BdbZIP genes
To probe the potential evolutionary mechanisms of BdbZIP gene family, according to described in  both tandem and segmental duplication events in terms of intragenome were examined in B. distachyon. It was observed that gene duplications were widespread throughout B. distachyon lineages (Figure 2). About 66% of BdbZIP genes were found to be duplicated at a maximal length of 100 kb. All the duplicated genes were confined to chromosomal block duplication and none of BdbZIP genes were found to be arranged in tandem form. The phenomena were very similar to the bZIP gene family in rice . This result further revealed why B. distachyon had high amount of bZIP genes.
Much evidence showed that CpG content and distribution might have influence on variability in chromatin structure and gene distribution . Based on this, we infered CpG content might affect the functional properties of BdbZIPs. To dig into the evolutionary relationships between BdbZIPs distribution and CpG content, we also counted the CpG content in the whole B. distachyon genome (Additional file 1: Table S5). The landscape of CpG content was generated and integrated to the genetic linkage map (Figure 2). It was observed that the distribution of CpG content was not uniform. Each chromosome had several relatively high CpG content regions (Figure 2). Except a few of BdbZIPs (BdbZIP5-7, 32–35, 65, 66, 73, and 83–87) were distributed in the regions of high CpG content, most of BdbZIP genes were scattered in the regions of low CpG content. This finding showed that those BdZIPs located in the regions of low CpG content might have high frequent mRNA transcripts, which required to implement their functions.
Phylogenetic and molecular evolutionary analysis of BdbZIP genes
Gene structure analysis of BdbZIP genes
Alternative splicing events were spread in the whole B. distachyon genome . As the overall pattern of intron position acted as an index to the phylogenetic relationships in a gene family evolution , so we also examined the intron and exon organization of BdbZIPs (Additional file 1: Table S4). It showed that most of BdbZIPs (81 of 96 BdbZIPs) containing introns, only 15 of total BdbZIP genes were intronless. As for the genes containing introns, the numbers of introns varied from 1 to 13. Diverse status of exon and intron splicing might be meaningful for BdbZIP gene evolution.
Dimerization properties of BdbZIP proteins
To evaluate the contribution of charged residues responsible for dimerization properties of BdbZIPs, the frequency of attractive and repulsive g↔e pairs in each heptad of BdbZIP leucine zippers was computed and the corresponding histogram was demonstrated (Figure 5C). It was found that the frequency of interactive g↔e pairs was the maximum in the first heptad, with a sharp decrease in the next three heptads (L2, L3, and L4). Then the trend increased in the fifth heptad and decreased sharply in the eighth heptad. Moreover, only repulsive g↔e pairs were observed in the eighth heptad and attractive g↔e pairs were observed in the ninth heptad. Attractive g↔e pairs and presence of Asns in a position contribute to homo-dimerization. Repulsive and incomplete g↔e pairs, and charged residues in a positions may favour hetero-dimerization. Based on this principle, all BdbZIPs were classified into three sub-families (sub-family I, II, and III, Additional file 3: Figure S2). According to above analyses, we observed that the dimerization patterns in the leucine zippers of BdbZIPs were more complex and diverse than those in other species. Our results indicated that there were many BdbZIPs with trends to form homo-dimerization.
BdbZIP proteins structure and expression patterns
Furthermore, we also investigated tissues/organs specific expression pattern of BdbZIPs genes. Four tissues/organs including root, stem, leaf, and early spikelet were selected. The –ΔΔCT changes and fold changes of 96 BdbZIP genes were calculated (Figure 6 and Additional file 1: Table S9). Our results showed that the expression levels of BdbZIP genes in four tissues/organs displayed with different patterns.
BdbZIP protein structure results showed that except for motif 1 and 7, most of motifs had just one copy. Certain motifs appeared in specific groups and some motifs were shared by several groups. This phenomenon might reflect the case that the functions of some conserved motifs were important and diverse in BdbZIPs. A large number of BdbZIP genes belonged to group I and II behaved high expression levels. Except some members in group III, IV, and V had higher expression, the expression for most of the BdbZIP genes in these three groups was relatively low. It should be noted that though some of BdbZIP genes with same structure were grouped to the same groups, the expression patterns were not completely consistent with the gene structural profiles. These results indicated that the structure of BdbZIP protein was not the single factor in determining their functions in different tissues/organs.
Stress expression analysis of BdbZIP genes
We also investigated whether the BdbZIP genes expression cluster had any enrichment with specific phylogenic clade genes, intron pattern, dimerization pattern or motif groups. It was observed that the expression of BdbZIPs in cluster II behaved heavy metal specific expression (Figure 7). We found that this cluster was composed of the high proportion of BdbZIPs belong to intron pattern b (46%), c (67%), d (67%), and e (50%). So we proposed that the 4 type of intron patterns were crucial in regulation of BdbZIPs responding to heavy metal stresses.
In order to further look BdbZIP genes expression pattern to specific group of treatments, we also did hierarchical cluster analysis of the BdbZIP genes expression according to environment factors, heavy metal stresses and phytohormone treatments respectively (Additional file 5: Figure S4, Additional file 6: Figure S5, Additional file 7: Figure S6).
Environmental factors (cold, heat, H2O2, PEG, and NaCl)
The proportion of down-regulated to up-regulated BdbZIP genes under environmental factors’ treatment was approximately 50% to 50%. Too high and low temperature were major negative factors on plant development due to the limiting the geographical locations suitable for plant growing and led to catastrophic loss of crop yield [58,59]. To uncover mechanism underlying temperature stresses, B. distachyon plants were subjected to heat and cold stress and a set of up- and down- regulated genes were identified, suggesting a prominent role for the bZIP genes responding to these environmental factors. Compared with the global analysis of the transcriptome of B. distachyon in cold, heat, drought and salt stress , 22 BdbZIPs were fell into 13 of 22 modules (Additional file 1: Table S11), which illustrated certain BdbZIPs were significant in processes of stress tolerance. Previous studies had shown that when rice was treated with cold, the bZIP genes OsbZIP14, 65, and 83 behaved down-regulated . The expression patterns of these OsbZIPs were similar to their homologous BdbZIP54, 63, and 80 respectively. Moreover, many evidences had proposed that excessive NaCl was toxic to plants, because NaCl caused cellular ion imbalances and hyperosmotic stress . So, we also examined the expression profiles of BdbZIPs under NaCl and osmotic (PEG) tolerance (Additional file 5: Figure S4 and Additional file 1: Table S10). In salt stress environment, the expressions of BdbZIP30 and BdbZIP41 were increased, which were very similar to their homologous OsbZIP63 and OsbZIP05 respectively .
Heavy metal stresses
With the development of industry, heavy metals contaminations are well known serious problems. Phytoremediation technologies including hyperaccumulation and uptake widely used to remove heavy metal pollutants are particularly important. Significant progresses have been made in recent years in native plants or genetic modified plants for phytoremediation of pollutants.
Genes associated with heavy metal tolerance or accumulation were identified in green alga, poplar, and maize [62-67]. To gain further insight of the potential roles of BdbZIPs may play in phytoremediation, we examined their expression patterns under heavy metals of Zn, Mn, Cu, Cd, and Pb. A series of BdbZIPs sensitive to heavy metal were detected (Additional file 6: Figure S5). Eighty percent of the BdbZIP genes were suppressed by heavy metal treatments (Additional file 6: Figure S5). The expression patterns of the BdbZIP genes under Zn and Mn were similar (Additional file 6: Figure S5).
It was notable that after dealing with heavy metals, there existed a few of BdbZIPs with high expression levels. Those BdbZIP genes with specific expression under heavy metal treatments might be potential for application of phytoremediation.
Phytohormones act as endogenous messengers when plants go through stress. During responding to environmental stresses, phytohormones such as auxin, ABA, salicylic acid, gibberellic acid play key roles and coordinate various signal transduction pathways . In plant treated with exogenous hormones, the genome-wide transcript profiles changed rapidly and transiently . Complex networks of transcription factors regulation by phytohormones under abiotic stresses had been reported . In this part, we treated B. distachyon seedlings with 4 types of phytohormones (SA, 6-BA, ABA, and MeJA) and investigated the BdbZIPs expression patterns. We found about 75% of BdbZIP genes were up-regulated upon these phytohormes treatments (Additional file 7: Figure S6). The expression profile of BdbZIP genes under SA and 6-BA treatments had similar expression patterns. The expression pattern of BdbZIP genes under ABA and MeJA were similar. Our findings showed that the expression patterns of BdbZIPs can be regulated by different phytohormones. So we proposed that stress tolerance of B. distachyon could be adjusted by applying different phytohormones.
Ninety six bZIP genes were first identified from the new grass model plant B.distachon. The BdbZIP genes chromosomal localization with gene duplication and CpG density were analyzed. Phylogenic analysis of these genes with their counterpart species of rice and Arabidopsis were investigated. Further characterization of bZIP domain of these genes in terms of exon splicing of basic and hinge region and identification of dimerization groups were performed. Finally, genes expression profiling of all BdbZIP genes upon 14 different stress conditions in B.distachon were obtained.
Most of the BdbZIP genes were located in the regions with low CpG density in chromosomes. BdbZIP gene duplications were widespread throughout the B. distachyon genome. Evolutionary analyses suggested that B. distachyon and monocot species have the similar evolutionary patterns, which lies two points: (1) B. distachyon and other monocot species maintained the similar and high number of bZIP genes, and (2) Seventy-five percent of total BdbZIPs have homologous genes in rice. bZIP domain characterization in terms of exon splicing of basic and hinge region and dimerization patterns of leucine zipper exhibited more complex and diverse than those in O. sativa and A. thalinana. All BdbZIP domains were classified into 3 major dimerization groups, and those BdbZIPs forming homo-dimerization were clustered into the same expression clusters.
Multiple stresses expression profile showed that BdbZIPs exhibited significant expression patterns, and those BdbZIPs responding to heavy metal treatments showed opposite expression pattern to those of the treatments of environmental factors and phytohormones. Certain BdbZIPs with expression level of fold changes ≥2 up- and down-regulated upon multiple-stress treatments were screened.
Abiotic stresses are important research areas of investigating mechanisms associated with crops yields under stress conditions. Identification of novel BdbZIP genes associated with stress tolerance and development of some strategies to obtain stress-tolerant plants are our currently major topics or future researches. Determination of the up-regulated, down-regulated, or stress specific BdbZIP genes, and utilizing the BdbZIP genes to improve productivity of grass plants and cereal crops upon complicated stress environment are crucial and significant.
This work was supported by grant for Starting Package to the Research Group of Plant Abiotic Stress and Plant Genome Evolution in Shanghai Chenshan Plant Science Research Centre, Chinese Academy of Sciences, and Shanghai Chenshan Botanic Garden from Shanghai Landscaping Administrative Bureau (NO. F0112423, F0122415, F122423, F132426).
- Liu JX, Srivastava R, Howell SH. Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis. Plant Cell Environ. 2008;31:1735–43.View ArticlePubMedGoogle Scholar
- Schlogl PS, Nogueira FT, Drummond R, Felix JM, De Rosa Jr VE, Vicentini R, et al. Identification of new ABA- and MEJA-activated sugarcane bZIP genes by data mining in the SUCEST database. Plant Cell Rep. 2008;27:335–45.View ArticlePubMedGoogle Scholar
- Yamamoto MP, Onodera Y, Touno SM, Takaiwa F. Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol. 2006;141:1694–707.View ArticlePubMed CentralPubMedGoogle Scholar
- Yang O, Popova OV, Suthoff U, Luking I, Dietz KJ, Golldack D. The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene. 2009;436:45–55.View ArticlePubMedGoogle Scholar
- Yang YG, Lv WT, Li MJ, Wang B, Sun DM, Deng X. Maize membrane-bound transcription factor Zmbzip17 Is a key regulator in the crosstalk of ER quality control and ABA signaling. Plant Cell Physiol. 2013;54:2020–33.View ArticlePubMedGoogle Scholar
- Hurst HC. Transcription factors. 1: bZIP proteins. Protein Profile. 1994;1:123–68.PubMedGoogle Scholar
- Ellenberger TE, Brandl CJ, Struhl K, Harrison SC. The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein-DNA complex. Cell. 1992;71:1223–37.View ArticlePubMedGoogle Scholar
- Vinson CR, Sigler PB, McKnight SL. Scissors-grip model for DNA recognition by a family of leucine zipper proteins. Science. 1989;246:911–6.View ArticlePubMedGoogle Scholar
- Fassler J, Landsman D, Acharya A, Moll JR, Bonovich M, Vinson C. B-ZIP proteins encoded by the Drosophila genome: evaluation of potential dimerization partners. Genome Res. 2002;12:1190–200.View ArticlePubMed CentralPubMedGoogle Scholar
- Nijhawan A, Jain M, Tyagi AK, Khurana JP. Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol. 2008;146:333–50.View ArticlePubMed CentralPubMedGoogle Scholar
- Wei KF, Chen J, Wang YM, Chen YH, Chen SX, Lin YN, et al. Genome-wide analysis of bZIP-encoding genes in maize. DNA Res. 2012;19:463–76.View ArticlePubMed CentralPubMedGoogle Scholar
- Fong JH, Keating AE, Singh M. Predicting specificity in bZIP coiled-coil protein interactions. Genome Biol. 2004;5:RII.View ArticleGoogle Scholar
- Newman JR, Keating AE. Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science. 2003;300:2097–101.View ArticlePubMedGoogle Scholar
- Vinson C, Myakishev M, Acharya A, Mir AA, Moll JR, Bonovich M. Classification of human B-ZIP proteins based on dimerization properties. Mol Cell Biol. 2002;22:6321–35.View ArticlePubMed CentralPubMedGoogle Scholar
- Deppmann CD, Acharya A, Rishi V, Wobbes B, Smeekens S, Taparowsky EJ, et al. Dimerization specificity of all 67 B-ZIP motifs in Arabidopsis thaliana: a comparison to homo sapiens B-ZIP motifs. Nucleic Acids Res. 2004;32:3435–45.View ArticlePubMed CentralPubMedGoogle Scholar
- Nardmann J, Werr W. The evolution of plant regulatory networks: what Arabidopsis cannot say for itself. Curr Opinion Plant Biol. 2007;10:653–9.View ArticleGoogle Scholar
- Xu F, Park MR, Kitazumi A, Herath V, Mohanty B, Yun SJ, et al. Cis- regulatory signatures of orthologous stress-associated bZIP transcription factors from rice, sorghum and Arabidopsis based on phylogenetic footprints. BMC Genomics. 2012;13:497–502.View ArticlePubMed CentralPubMedGoogle Scholar
- Correa LGG, Riano-Pachon DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M. The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder. PLoS One. 2008;3:e2944.View ArticlePubMed CentralPubMedGoogle Scholar
- Mahajan S, Tuteja N. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys. 2005;444:139–58.View ArticlePubMedGoogle Scholar
- Xiong L, Schumaker KS, Zhu JK. Cell signaling during cold, drought, and salt stress. Plant Cell. 2002;14 (Suppl):S165–83.Google Scholar
- Urano K, Kurihara Y, Seki M, Shinozaki K. ‘Omics’ analyses of regulatory networks in plant abiotic stress responses. Curr Opin Plant Biol. 2010;13:132–8.View ArticlePubMedGoogle Scholar
- Zhang H, Jin JP, Tang L, Zhao Y, Gu XC, Gao G, et al. PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res. 2011;39(Database issue):1114–7.View ArticleGoogle Scholar
- Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, et al. bZIP transcription factors in Arabidopsis. Trends Plant Sci. 2002;7:106–11.View ArticlePubMedGoogle Scholar
- Baloglu MC, Eldem V, Hajyzadeh M, Unver T. Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS One. 2014;9:e96014.View ArticlePubMed CentralPubMedGoogle Scholar
- Wang JZ, Zhou JX, Zhang BL, Vanitha J, Ramachandran S, Jiang SY. Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum. J Integr Plant Biol. 2011;53:212–31.View ArticlePubMedGoogle Scholar
- Liu JY, Chen NN, Chen F, Cai B, Santo SD, Tornielli GB, et al. Genome-wide analysis and expression profile of bZIP transcription factor gene family in grapevine (Vitis vinifera). BMC Genomics. 2014;15:281–99.View ArticlePubMed CentralPubMedGoogle Scholar
- Liu CT, Mao BG, Ou SJ, Wang W, Liu LC, Wu YB, et al. OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol. 2014;84:19–36.View ArticlePubMedGoogle Scholar
- Tang N, Zhang H, Li XH, Xiao JH, Xiong LZ. Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol. 2012;158:1755–68.View ArticlePubMed CentralPubMedGoogle Scholar
- Liu CT, Wu YB, Wang XP. bZIP transcription factor OsbZIP52/RISBZ5: a potential negative regulator of cold and drought stress response in rice. Planta. 2012;235:1157–69.View ArticlePubMedGoogle Scholar
- Finkelstein RR, Lynch TJ. The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell. 2000;12:599–609.View ArticlePubMed CentralPubMedGoogle Scholar
- Ji XY, Liu GF, Liu YJ, Zheng L, Nie XG, Wang YG. The bZIP protein from Tamarix hispida, ThbZIP1, is ACGT elements binding factor that enhances abiotic stress signaling in transgenic Arabidopsis. BMC Plant Biol. 2013;13:151–64.View ArticlePubMed CentralPubMedGoogle Scholar
- He S, Shan W, Kuang JF, Xie H, Xiao YY, Lu WJ, et al. Molecular characterization of a stress-response bZIP transcription factor in banana. Plant Cell Tiss Org Cult. 2013;113:173–87.View ArticleGoogle Scholar
- Al-Najar H, Kaschl A, Schulz R, Romheld V. Effect of thallium fractions in the soil and pollution origins on Tl uptake by hyperaccumulator plants: a key factor for the assessment of phytoextraction. Int J Phytoremediation. 2005;7:55–67.View ArticlePubMedGoogle Scholar
- Anderson L, Walsh MM. Arsenic uptake by common marsh fern Thelypteris palustris and its potential for phytoremediation. Sci Total Environ. 2007;379:263–5.View ArticlePubMedGoogle Scholar
- Chandra R, Yadav S. Phytoremediation of Cd, Cr, Cu, Mn, Fe, Ni, Pb and Zn from aqueous solution using Phragmites cummunis, Typha angustifolia and Cyperus esculentus. Int J Phytoremediation. 2011;13:580–91.View ArticlePubMedGoogle Scholar
- Gupta DK, Huang HG, Corpas FJ. Lead tolerance in plants: strategies for phytoremediation. Environ Sci Pollut Res Int. 2013;20:2150–61.View ArticlePubMedGoogle Scholar
- Hussein HS, Ruiz ON, Terry N, Daniell H. Phytoremediation of mercury and organomercurials in chloroplast transgenic plants: enhanced root uptake, translocation to shoots, and volatilization. Environ Sci Technol. 2007;41:8439–46.View ArticlePubMed CentralPubMedGoogle Scholar
- Jacob DL, Borchardt JD, Navaratnam L, Otte ML, Bezbaruah AN. Uptake and translocation of Ti from nanoparticles in crops and wetland plants. Int J Phytoremed. 2013;15:142–53.View ArticleGoogle Scholar
- Pineau C, Loubet S, Lefoulon C, Chalies C, Fizames C, Lacombe B, et al. Natural variation at the FRD3 MATE transporter locus reveals cross-talk between Fe homeostasis and Zn tolerance in Arabidopsis thaliana. PLoS Genet. 2012;8:e1003120.View ArticlePubMed CentralPubMedGoogle Scholar
- International Brachypodium I. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature. 2010;463:763–8.View ArticleGoogle Scholar
- Alves SC, Worland B, Thole V, Snape JW, Bevan MW, Vain P. A protocol for Agrobacterium-mediated transformation of Brachypodium distachyon community standard line Bd21. Nat Protoc. 2009;4:638–49.View ArticlePubMedGoogle Scholar
- Trabucco GM, Matos DA, Lee SJ, Saathoff AJ, Priest HD, Mockler TC, et al. Functional characterization of cinnamyl alcohol dehydrogenase and caffeic acid O-methyltransferase in Brachypodium distachyon. BMC Biotechnol. 2013;13:61–80.View ArticlePubMed CentralPubMedGoogle Scholar
- Trafford K, Haleux P, Henderson M, Parker M, Shirley NJ, Tucker MR, et al. Grain development in Brachypodium and other grasses: possible interactions between cell expansion, starch deposition, and cell-wall synthesis. J Exp Bot. 2013;64:5033–47.View ArticlePubMedGoogle Scholar
- Verelst W, Bertolini E, De Bodt S, Vandepoele K, Demeulenaere M, Pe ME, et al. Molecular and physiological analysis of growth-limiting drought stress in Brachypodium distachyon leaves. Mol Plant. 2013;6:311–22.View ArticlePubMedGoogle Scholar
- Priest HD, Fox SE, Rowley ER, Murray JR, Michael TP, Mockler TC. Analysis of global gene expression in Brachypodium distachyon reveals extensive network plasticity in response to abiotic stress. PLoS One. 2014;9:e87499.View ArticlePubMed CentralPubMedGoogle Scholar
- Reinke AW, Baek J, Ashenberg O, Keating AE. Networks of bZIP protein-protein interactions diversified over a billion years of evolution. Science. 2013;340:730–4.View ArticlePubMed CentralPubMedGoogle Scholar
- Jin JP, Zhang H, Kong L, Gao G, Luo JC. PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res. 2013;42(Database issue):1182–7.Google Scholar
- Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011;28:2731–9.View ArticlePubMed CentralPubMedGoogle Scholar
- Lee TH, Tang HB, Wang XY, Paterson AH. PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res. 2013. doi:10.1093/nar/gks1104.Google Scholar
- Liu RH, Meng JL. MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas. 2003;25:317–21.PubMedGoogle Scholar
- Liu X, Zuo KJ, Xu JT, Li Y, Zhang F, Yao HY, et al. Functional analysis of GbAGL1, a D-lineage gene from cotton (Gossypium barbadense). J Exp Bot. 2010;61:1193–203.View ArticlePubMed CentralPubMedGoogle Scholar
- Cannon SB, Mitra A, Baumgarten A, Young ND, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4:10.View ArticlePubMed CentralPubMedGoogle Scholar
- Paterson AH, Bowers JE, Chapman BA. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc Natl Acad Sci U S A. 2004;101:9903–8.View ArticlePubMed CentralPubMedGoogle Scholar
- Arndt PF, Hwa T, Petrov DA. Substantial regional variation in substitution rates in the human genome: importance of GC content, gene density, and telomere-specific effects. J Mol Evol. 2005;60:748–63.View ArticlePubMedGoogle Scholar
- Walters B, Lum G, Sablok G, Min XJ. Genome-wide landscape of alternative splicing events in Brachypodium distachyon. DNA Res. 2013;20:163–71.View ArticlePubMed CentralPubMedGoogle Scholar
- Patthy L. Intron-dependent evolution: preferred types of exons and introns. FEBS Lett. 1987;214:1–7.View ArticlePubMedGoogle Scholar
- Acharya A, Ruvinov SB, Gal J, Moll JR, Vinson C. A heterodimerizing leucine zipper coiled coil system for examining the specificity of a position interactions: amino acids I, V, L, N, A, and K. Biochemistry. 2002;41:14122–31.View ArticlePubMedGoogle Scholar
- Bita CE, Gerats T. Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci. 2013;4:273.View ArticlePubMed CentralPubMedGoogle Scholar
- Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:571–99.View ArticlePubMedGoogle Scholar
- Wang D, Pan YJ, Zhao XQ, Zhu LH, FU BY, Li ZK. Genome-wide temporal-spatial gene expression profiling of drought responsiveness in rice. BMC Genomics. 2011;12:149.View ArticlePubMed CentralPubMedGoogle Scholar
- Zhu JK. Plant salt tolerance. Trends Plant Sci. 2001;6:66–71.View ArticlePubMedGoogle Scholar
- Ding D, Li W, Song G, Qi H, Liu J, Tang J. Identification of QTLs for arsenic accumulation in maize. (Zea mays L.) using a RIL population. PLoS One. 2011;6:e25646.View ArticlePubMed CentralPubMedGoogle Scholar
- Kieffer P, Dommes J, Hoffmann L, Hausman JF, Renaut J. Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics. 2008;8:2514–30.View ArticlePubMedGoogle Scholar
- Mendoza-Cozatl DG, Jobe TO, Hauser F, Schroeder JI. Long-distance transport, vacuolar sequestration, tolerance, and transcriptional responses induced by cadmium and arsenic. Curr Opin Plant Biol. 2011;14:554–62.View ArticlePubMed CentralPubMedGoogle Scholar
- Quaggiotti S, Barcaccia G, Schiavon M, Nicole S, Galla G, Rossignolo V, et al. Phytoremediation of chromium using Salix species: cloning ESTs and candidate genes involved in the Cr response. Gene. 2007;402:68–80.View ArticlePubMedGoogle Scholar
- Rubinelli P, Siripornadulsil S, Gao-Rubinelli F, Sayre RT. Cadmium- and iron-stress-inducible gene expression in the green alga Chlamydomonas reinhardtii: evidence for H43 protein function in iron assimilation. Planta. 2002;215:1–13.View ArticlePubMedGoogle Scholar
- Shen YO, Zhang YZ, Chen J, Lin HJ, Zhao MJ, Peng HW, et al. Genome expression profile analysis reveals important transcripts in maize roots responding to the stress of heavy metal Pb. Physiol Plant. 2013;147:270–82.View ArticlePubMedGoogle Scholar
- Wolters H, Jurgens G. Survival of the flexible: hormonal growth control and adaptation in plant development. Nat Rev Genet. 2009;10:305–17.View ArticlePubMedGoogle Scholar
- Chapman EJ, Estelle M. Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet. 2009;43:265–85.View ArticlePubMedGoogle Scholar
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