- Research article
- Open Access
Genomic, expressional, protein-protein interactional analysis of Trihelix transcription factor genes in Setaria italia and inference of their evolutionary trajectory
- Zhenyi Wang†1, 2Email author,
- Kanglu Zhao†1,
- Yuxin Pan†1, 2,
- Jinpeng Wang†1, 2,
- Xiaoming Song†1, 2,
- Weina Ge†1, 2,
- Min Yuan1, 2,
- Tianyu Lei1, 2,
- Li Wang1, 2,
- Lan Zhang1, 2,
- Yuxian Li1, 2,
- Tao Liu2, 3,
- Wei Chen2, 3,
- Wenjing Meng1,
- Changkai Sun1,
- Xiaobo Cui1,
- Yun Bai1 and
- Xiyin Wang1, 2Email author
© The Author(s). 2018
- Received: 17 May 2018
- Accepted: 31 August 2018
- Published: 12 September 2018
Trihelix transcription factors (TTF) play important roles in plant growth and response to adversity stress. Until now, genome-wide identification and analysis of this gene family in foxtail millet has not been available. Here, we identified TTF genes in the foxtail millet and its grass relatives, and characterized their functional domains.
As to sequence divergence, TTF genes were previously divided into five subfamilies, I-V. We found that Trihelix family members in foxtail millet and other grasses mostly preserved their ancestral chromosomal locations during millions of years’ evolution. Six amino acid sites of the SIP1 subfamily possibly were likely subjected to significant positive selection. Highest expression level was observed in the spica, with the SIP1 subfamily having highest expression level. As to the origination and expansion of the gene family, notably we showed that a subgroup of subfamily IV was the oldest, and therefore was separated to define a new subfamily O. Overtime, starting from the subfamily O, certain genes evolved to form subfamilies III and I, and later from subfamily I to develop subfamilies II and V. The oldest gene, Si1g016284, has the most structural changes, and a high expression in different tissues. What’s more interesting is that it may have bridge the interaction with different proteins.
By performing phylogenetic analysis using non-plant species, notably we showed that a subgroup of subfamily IV was the oldest, and therefore was separated to define a new subfamily O. Starting from the subfamily O, certain genes evolved to form other subfamilies. Our work will contribute to understanding the structural and functional innovation of Trihelix transcription factor, and the evolutionary trajectory.
- Foxtail millet
- Transcription factor
Transcription factor is a type of DNA binding protein, and interacts with cis element of promoter regions of target genes, regulating the expression of them. At present, more than 60 transcription factor families have been found in plants . Trihelix transcription factor is among the earliest transcription factor families discovered in plants .
Trihelix transcription factors (TTF) feature a conservative domain containing three series of alpha helix structure [2, 3]. TTFs were reported to play multiple regulatory roles in plant growth, development process, and response to adversity stress [4–7]. According to the changes in their alpha helix domain , they were previously divided into five subfamilies, respectively referring as I(or SH4), II(or GT-1), III(or GTγ), IV(or SIP1), and V(or GT-2). Each subfamily was named as to their respective first member found. Pea (Pisumsativum l.) GT-1 factor is the earliest identified TTF, which specifically combined with GT elements of light-induced gene rbcS–3A’s promoter . In tobacco (Nicotiana tabacum) , Arabidopsis (Arabidopsis thaliana) , and rice (Oryza sativa) , homologous GT-1 genes were cloned. GT-2 was the first GT-factor isolated, containing two separate Trihelix domains [9, 10], each involved in DNA binding. Arabidopsis’s ETAL LOSS (PTL) gene belongs to the GT-2 family, and can regulate the growth of petals and sepals. It was also found to regulate flower organ formation of shape [11–13]. Rice SHATTERING1 (SHA1) gene, encoding a SH4 type of transcription factor, is the only identified member found in the SH4 subfamily, playing an important role in cell differentiation activation. A mutant SHA1 gene was found to cause the disappearance of the seed holding in rice . GTγ subfamily has four members identified in rice, OsGTγ-1、OsGTγ-2、OsGTγ-3, and OsGTγ-4, which were related to cold, drought, and salt stress response . Certain SIP1 genes have been identified in the tobacco and Arabidopsis, related to the development of plant embryo, leaf development, and cell proliferation [16–18]. Recently, expression profiles of Trihelix genes were available in tomato  and Populus trichocarpa, under biotic and abiotic stresses in the latter . A new gene BnSIP1 was discovered in Brassica napus  mediating abiotic stress tolerance and ABA signaling.
Foxtail millet (Setaria italica) is one important arid and semi-arid crop, being a staple diet for people in some regions in China, India, and other Asian countries. Owing to its economic importance, its genome was sequenced [22, 23], together with further sequencing efforts [24–27], providing a rich genomic and genetic resources for biological research and breeding practice . These precious efforts and accumulating resources empower researches in the Setaria community. Recently, tens of researches were performed to understand key functional gene families of the crop [29–43]. These researches described certain important transcription factor genes and gene families, such as Dof genes, encoding a class of transcription factors involved in numerous physiological and biochemical reactions affecting growth and development , TRANSPARENT TESTA GLABRA 1 genes, encoding a WD40 repeat transcription factor with multiple roles in plant growth and development, particularly in seed metabolite production , lipid transfer protein genes (LTPs), encoding a class of cysteine-rich soluble proteins having small molecular weights , MYB genes , APETALA2/ethylene-responsive element binding factor (AP2/ERF) genes , NAC genes  and so on .
Here, we identified TTF genes in foxtail millet, and characterized their molecular characteristic, genome distribution, and possible biological function. Moreover, by performing an evolutionary genomics analysis in selected plants, moss, green algaes, and yeast, we explored the evolution and origin of the TTF genes and inferred their possible evolutionary trajectories about their origin and divergence.
Genome data of foxtail millet, rice, and sorghum were downloaded from JGI database (http://genome.jgi.doe.gov/). To identify putative Trihelix family members, the Hidden Markov Model (HMM) profiles of Trihelix (PF13837) were retained from the Pfam database (http://pfam.xfam.org/) and were used to identify the putative Trihelix proteins with the best domain e-value cutoffs of < 1 × 10− 4. The rice Trihelix sequences  were used as the query to perform a BLASTP search in these species , with a cutoff e-value of< 10− 10. By using SMART program  (http://smart.embl-heidelberg.de/) and the National Center for Biotechnology Information (NCBI) database (http://www.ncbi.nlm.nih.gov/), we detected the candidate protein by characterizing the typical Trihelix feature structure domain. We checked the ExPASy database (http://www.expasy.org/) to retrieve information as molecular weight, isoelectric point of TTF proteins . Based on the above method and TFDB 4.0 database (http://planttfdb.cbi.pku.edu.cn/) , we obtained TTF homologs from other species: Ae. tauschii, T. urartu, barley, Brachypodium, maize, Saccharomyces cerevisiae, Chlamydomonas reinhardtii, Coccomyxa subellipsoidea, Volvox carteri, Physcomitrella patens, and Selaginella moellendorffii.
Gene structure analysis
According to the downloaded gff3 annotation file, the required data is extracted and the format is modified by the home-made Perl program. By using GSDS 2.0 (http://gsds.cbi.pku.edu.cn/), we analyzed genetic structure of TTF genes .
By using protein conservative motif online search program MEME 4.11.3 (http://meme-suite.org/tools/meme), we analyzed conservative motif of TTF gene family, and set the relevant parameters of motif repeat number to be “any”, motif length to be 6 ~ 200 aa, and motif prediction number to be 25 [52, 53]. By using WebLogo 3.6.0 (http://weblogo.threeplusone.com/), we characterized conservative region in amino acid sequence .
Gene localization and divergence
We used BioPerl program to estimate synonymous nucleotide substitution per synonymous site (Ks), and then drawing the circle diagram through the home-made Python program. All millet Trihelix genes are noted in the chromosome, genome evolution homologous duplicate events are connected by color lines with Ks. Ks: 0–0.35 black; 0.35–0.45 green; 0.45–0.65 red; 0.65–2 blue .
Multiple sequence alignment and evolutionary tree construction
Multiple sequence alignment of millet, rice, sorghum, Ae. tauschii, T.urartu, barley, Brachypodium and maize TTF gene family were performed by using Clustal X version 2.0 . According to the sequence alignment, phylogenetic tree of TTF genes were built by PHYLIP 3.695 program with the Neighbor-joining method (http://evolution.genetics.washington.edu/phylip.html), and the Bootstrap value 1000 was adopted.
Selection pressure analysis
Using PAML 4.8 Codeml program (http://abacus.gene.ucl.ac.uk/software/paml.html), we tested whether the sequences to bear the positive selection with four comparison models of M1a, M2a, M7, and M8 .
Orthologs in foxtail millet, rice and sorghum
Using OrthoMCL program (http://orthomcl.org/orthomcl/) , we analyzed chromosome segments duplication between foxtail millet, rice, and sorghum Trihelix genes, with the default settings, which initially required an all-against-all BLASTP, and then the relationships between the genes were deduced by the MCL clustering algorithm. The result is graphic by Circos software (http://circos.ca/) .
Transcriptome and RNA - seq data was downloaded from the foxtail millet database (http://foxtailmillet.genomics.org.cn/page/species/index.jsp), and TTF expression data extracted by using home-made Perl program. The foxtail millet TTF genes expression cluster from each tissue was analyzed using Cluster 3.0 software (http://bonsai.hgc.jp/~mdehoon/software/cluster/software.htm), and the RPKM values were log2 transformed. The heat map of hierarchical clustering was visualized with TreeView1.1.3.
Protein interaction network
We used STRING 10.5 database (http://string.embl.de/)  to analyze millet TTF interaction with other foxtail millet proteins. We set the minimum required interaction score to be high confidence (0.700), and max number of interactors to be 5.
Identification and genomic distribution
We identified 27 TTF genes in the foxtail millet genome database (Additional file 1: Table S1). The shortest sequence has 212 amino acid residues, while the longest one has 878 amino acid residues. The estimated protein molecular weights fall in a range 23,453.7~ 96,360.6, and the isoelectric points in a range 4.9184~ 11.2729.
The predicted 27 millet TTF genes have 36 transcripts (Additional file 2: Figure S1). Twenty-one genes (21 or 77.8%) were found to have a single transcript, while 6 of them have multiple transcripts, with Si7g009787 having the most (5). They have considerably divergent genic structures, with 1–17 exons. For example, 12 genes, e.g., Si6g014062, Si9g036682, have a single exon, while the gene Si1g016284 has 17 exons and its gene structure is broken into short pieces by inserted introns.
In foxtail millet, TTF genes in each subfamily have similar motif (Fig. 1). All six subfamily III genes contain Motif 4. The subfamilies I and IV feature the containing of Motif 8 and 9 while the subfamily II and the subfamily V features Motif 2.
TTF genes contain a conservative structure domain in the N terminal (except Si1g016284) (Fig. 1), while GT-2 contains the domain structure in the C terminal and 2 repeatitive and conservative structure domain. The GT-1 and GT-2 subfamilies are much more similar than to other subfamilies.
With the exception of Si1g016284, the other genes contain a conservative domain near the N-terminal, in which 1/5 of the amino acid residues are quite conservative, with Trp (W) - 1, Trp (W) - 64 and Cys(C) - 100 being highly conserved (Additional file 4: Figure S2).
Evolutionary establishment of the family
Natural selection pressure analysis
Pr (w > 1)
post mean for w
Expression profile in the different organs
In addition, expression has been down-regulated in many structurally variable genes. Si9g040176 had more copies of Motif 9 than others in subfamily I, possibly subjected a recent motif addition and is down-regulated. In subfamily III Si8g026391 had fewer copies of Motif 21 than the genes Si7g010102, and Si9g037484 had the simplest structure in the subfamily IV indicating a motif deletion, and they are also down-regulated. In the subfamily V, compared to other genes, Si2g033157 lost the domain in the C terminal region, and it is down-regulated. In contrast, though Si7g009787, having the most transcripts, and Si1g016284, being the oldest gene in the family, are each variable in structure, they had higher expression, showing possible functional benefit of plants due to their variable structure.
The oldest TTF gene, Si1g016284, played a significant role in the interaction. It seems to serve as a bridge connecting the Trihelix family and other millet proteins, and is co-expressed with many proteins (6), suggesting that these proteins function synergistically. Structurally, Si1g016284 has two extra domains, Lactamase_B and RMMBL, in addition to the characteristic of the Trihelix family. The five non-Trihelix proteins interacting with it have variable domains, such as Lactamase_B, RMMBL, Beta_Casp, CPSF100_C, WD40, ZnF_C3H1, YTH, and/or HAT, showing a multiple-facet nature of Silg016284.
As a multi-functional transcription factor family, TTFs were the first ones identified in plants . Here, starting from research in foxtail millet and extending into other organisms, we explored their functional changes, expressional features, genomic duplication and phylogenetics. Eventually, we identified an oldest subfamily, referred as O, in the constructed phylogenetic tree. Interestingly, the single foxtail millet gene Si1g016284 in subfamily O is the one having the most exons (Additional file 2: Figure S1). It has a single ortholog in yeast or any algae species, and two orthologs in fern and three orthologs in moss. Actually, this seems to be weird in that we would have expected that it might be the most conservative one to have highest similarity with the homologs from far diverged life domains. This shows that, though broken into 17 segments, the gene might have not been pseudogenized but rather likely functional.
Starting from the subfamily O, primitive TTF genes continued to expand in the plant domain. As to the reconstructed tree topology, we found that certain genes evolved to form subfamilies III and I, and later from subfamily I to develop subfamilies II and V (Fig. 5).
In each subfamily, there is evidence that genome duplications contributed to accumulate more copies. For example, in foxtail millet, a group of genes in subfamily IV appeared after its divergence from other grasses (Fig. 3), and moss has the most TTF genes with new copies seemingly having been continuously produced (Fig. 5).
The primitive TTF gene, Si1g016284, has conserved domain in its C terminal region, as genes forming subfamily O from different life domains. Contrastively, the conserved domains were found in N terminal or both terminals in the other foxtail millet genes (Fig. 1).
Besides, subfamily GTγ were not found in Lycophta and S. Moellendorffii (Fig. 5), consistent to previous report . This shows that though as an old subfamily, they may have been pseudogenized or removed from certain plants.
TTF genes were previously divided into five subfamilies, I-V. By performing phylogenetic analysis using non-plant species, notably we showed that a subgroup of subfamily IV was the oldest, and therefore was separated to define a new subfamily O. Starting from the subfamily O, certain genes evolved to form other subfamilies. The oldest gene, Si1g016284, has the most structural changes, and a high expression in different tissues. What’s more interesting is that it may have bridge the interaction with different proteins. Our work will contribute to understanding the structural and functional innovation of Trihelix transcription factor, and the evolutionary trajectory.
We thank the center for genomics and computational biology lab team for discussion and support.
This work was supported by the Youth Foundation of Educational Committee of Hebei Province (grant no. QN2017123), Undergraduate Training Programs for Innovation and Entrepreneurship of North China University of Science and Technology (grant no. X2016161) to KZ, National Natural Science Foundation of China (grant no. 31371282) to XW, National Natural Science Foundation of China (grant no. 31501072) to TL, National Science Foundation of Hebei province (grant no. C2016209097) to WG, China-Hebei 100 Scholars Supporting Project (grant no. E2013100003) to XW.
Availability of data and materials
All data generated or analyzed during this study were included in this published article and the Additional files. We have been using public data and do not have produced sequence data by ourselves.
XW, ZW and KZ designed the experiments and organized the manuscript. ZW, KZ, XS, WG, JW, MY, TL, LW, LZ, YL, TL, WC, WM, CS, XC, YB, YP and XW performed the experiments. ZW and KZ wrote the manuscript. XW, YP and XS edited the manuscript. All the authors discussed the results and contributed to the manuscript. All authors read and approved the final manuscript.
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